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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.

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.

Tresguerres, M, Barott K, Barron ME, Deheyn D, Kline D, Linsmayer LB.  2017.  Cell Biology of Reef-Building Corals: Ion Transport, Acid/Base Regulation, and Energy Metabolism. Acid-Base Balance and Nitrogen Excretion in Invertebrates. ( Weihrauch D, O'Donnell M, Eds.).:193-218.: Springer International Publishing   10.1007/978-3-319-39617-0_7   Abstract

Coral reefs are built by colonial cnidarians that establish a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium. The processes of photosynthesis, calcification, and general metabolism require the transport of diverse ions across several cellular membranes and generate waste products that induce acid/base and oxidative stress. This chapter reviews the current knowledge on coral cell biology with a focus on ion transport and acid/base regulation while also discussing related aspects of coral energy metabolism.

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Nash, MC, Opdyke BN, Troitzsch U, Russell BD, Adey WH, Kato A, Diaz-Pulido G, Brent C, Gardner M, Prichard J, Kline DI.  2013.  Dolomite rich coral reef coralline algae resist dissolution in acidified conditions.. Nature Climate Change. 3:268-272.   10.1038/nclimate1760   Abstract

Coral reef ecosystems develop best in high-flow environments but their fragile frameworks are also vulnerable to high wave energy. Wave-resistant algal rims, predominantly made up of the crustose coralline algae (CCA) Porolithon onkodes and P. pachydermum1, 2, are therefore critical structural elements for the survival of many shallow coral reefs. Concerns are growing about the susceptibility of CCA to ocean acidification because CCA Mg-calcite skeletons are more susceptible to dissolution under low pH conditions than coral aragonite skeletons3. However, the recent discovery4 of dolomite (Mg0.5Ca0.5(CO3)), a stable carbonate5, in P. onkodes cells necessitates a reappraisal of the impacts of ocean acidification on these CCA. Here we show, using a dissolution experiment, that dried dolomite-rich CCA have 6–10 times lower rates of dissolution than predominantly Mg-calcite CCA in both high-CO2 (~ 700 ppm) and control (~ 380 ppm) environments, respectively. We reveal this stabilizing mechanism to be a combination of reduced porosity due to dolomite infilling and selective dissolution of other carbonate minerals. Physical break-up proceeds by dissolution of Mg-calcite walls until the dolomitized cell eventually drops out intact. Dolomite-rich CCA frameworks are common in shallow coral reefs globally and our results suggest that it is likely that they will continue to provide protection and stability for coral reef frameworks as CO2

Hamilton, TJ, Tresguerres M, Kline DI.  2017.  Dopamine D1 receptor activation leads to object recognition memory in a coral reef fish. Biology Letters. 13   10.1098/rsbl.2017.0183   Abstract

Object recognition memory is the ability to identify previously seen objects and is an adaptive mechanism that increases survival for many species throughout the animal kingdom. Previously believed to be possessed by only the highest order mammals, it is now becoming clear that fish are also capable of this type of memory formation. Similar to the mammalian hippocampus, the dorsolateral pallium regulates distinct memory processes and is modulated by neurotransmitters such as dopamine. Caribbean bicolour damselfish (Stegastes partitus) live in complex environments dominated by coral reef structures and thus likely possess many types of complex memory abilities including object recognition. This study used a novel object recognition test in which fish were first presented two identical objects, then after a retention interval of 10 min with no objects, the fish were presented with a novel object and one of the objects they had previously encountered in the first trial. We demonstrate that the dopamine D1-receptor agonist (SKF 38393) induces the formation of object recognition memories in these fish. Thus, our results suggest that dopamine-receptor mediated enhancement of spatial memory formation in fish represents an evolutionarily conserved mechanism in vertebrates.

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Nash, MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI.  2011.  First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences. 8:3331-3340.   10.5194/bg-8-3331-2011   AbstractWebsite

Dolomite is a magnesium-rich carbonate mineral abundant in fossil carbonate reef platforms but surprisingly rare in modern sedimentary environments, a conundrum known as the "Dolomite Problem". Marine sedimentary dolomite has been interpreted to form by an unconfirmed, post-depositional diagenetic process, despite minimal experimental success at replicating this. Here we show that dolomite, accompanied by magnesite, forms within living crustose coralline alga, Hydrolithon onkodes, a prolific global tropical reef species. Chemical micro-analysis of the coralline skeleton reveals that not only are the cell walls calcitised, but that cell spaces are typically filled with magnesite, rimmed by dolomite, or both. Mineralogy was confirmed by X-ray Diffraction. Thus there are at least three mineral phases present (magnesium calcite, dolomite and magnesite) rather than one or two (magnesium calcite and brucite) as previously thought. Our results are consistent with dolomite occurrences in coralline algae rich environments in fossil reefs of the last 60 million years. We reveal that the standard method of removing organic material prior to Xray Diffraction analysis can result in a decrease in the most obvious dolomite and magnesite diffraction patterns and this may explain why the abundant protodolomite and magnesite discovered in this study has not previously been recognized. This discovery of dolomite in living coralline algae extends the range of palaeo-environments for which biologically initiated dolomite can be considered a possible source of primary dolomite.

Gattuso, JP, Kirkwood W, Barry JP, Cox E, Gazeau F, Hansson L, Hendriks I, Kline DI, Mahacek P, Martin S, McElhany P, Peltzer ET, Reeve J, Roberts D, Saderne V, Tait K, Widdicombe S, Brewer PG.  2014.  Free-ocean CO2 enrichment (FOCE) systems: present status and future developments. Biogeosciences. 11:4057-4075.   10.5194/bg-11-4057-2014   AbstractWebsite

Free-ocean CO2 enrichment (FOCE) systems are designed to assess the impact of ocean acidification on biological communities in situ for extended periods of time (weeks to months). They overcome some of the drawbacks of laboratory experiments and field observations by enabling (1) precise control of CO2 enrichment by monitoring pH as an offset of ambient pH, (2) consideration of indirect effects such as those mediated through interspecific relationships and food webs, and (3) relatively long experiments with intact communities. Bringing perturbation experiments from the laboratory to the field is, however, extremely challenging. The main goal of this paper is to provide guidelines on the general design, engineering, and sensor options required to conduct FOCE experiments. Another goal is to introduce xFOCE, a community-led initiative to promote awareness, provide resources for in situ perturbation experiments, and build a user community. Present and existing FOCE systems are briefly described and examples of data collected presented. Future developments are also addressed as it is anticipated that the next generation of FOCE systems will include, in addition to pH, options for oxygen and/or temperature control. FOCE systems should become an important experimental approach for projecting the future response of marine ecosystems to environmental change.

Dove, SG, Kline DI, Pantos O, Angly FE, Tyson GW, Hoegh-Guldberg O.  2013.  Future reef decalcification under a business-as-usual CO2 emission scenario. Proceedings of the National Academy of Sciences. 110:15342-15347.   10.1073/pnas.1302701110   AbstractWebsite

Increasing atmospheric partial pressure of CO2 (pCO2) is a major threat to coral reefs, but some argue that the threat is mitigated by factors such as the variability in the response of coral calcification to acidification, differences in bleaching susceptibility, and the potential for rapid adaptation to anthropogenic warming. However the evidence for these mitigating factors tends to involve experimental studies on corals, as opposed to coral reefs, and rarely includes the influence of multiple variables (e.g., temperature and acidification) within regimes that include diurnal and seasonal variability. Here, we demonstrate that the inclusion of all these factors results in the decalcification of patch-reefs under business-as-usual scenarios and reduced, although positive, calcification under reduced-emission scenarios. Primary productivity was found to remain constant across all scenarios, despite significant bleaching and coral mortality under both future scenarios. Daylight calcification decreased and nocturnal decalcification increased sharply from the preindustrial and control conditions to the future scenarios of low (reduced emissions) and high (business-as-usual) increases in pCO2. These changes coincided with deeply negative carbonate budgets, a shift toward smaller carbonate sediments, and an increase in the abundance of sediment microbes under the business-as-usual emission scenario. Experimental coral reefs demonstrated highest net calcification rates and lowest rates of coral mortality under preindustrial conditions, suggesting that reef processes may not have been able to keep pace with the relatively minor environmental changes that have occurred during the last century. Taken together, our results have serious implications for the future of coral reefs under business-as-usual environmental changes projected for the coming decades and century.

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Beijbom, O, Treibitz T, Kline DI, Eyal G, Khen A, Neal B, Loya Y, Mitchell GB, Kriegman D.  2016.  Improving automated annotation of benthic survey images using wide-band fluorescence. Scientific reports. 6:23166.: Nature Publishing Group Abstract
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Calamia, MA, Kline DI, Kago S, Donovan K, Dulunaqio S, Tabaleka T, Mitchell BG.  2010.  Marine-based community conserved areas in Fiji: an example of indigenous governance and partnership. Indigenous peoples and conservation: from rights to resource management. ( Walker Painemilla K, Rylands AB, Woofter A, Hughers C, Eds.).:95-114., Arlington, VA.: Conservation International Abstract
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Neal, BP, Lin TH, Winter RN, Treibitz T, Beijbom O, Kriegman D, Kline DI, Mitchell BG.  2015.  Methods and measurement variance for field estimations of coral colony planar area using underwater photographs and semi-automated image. Environmental Monitoring and Assessment. 187   10.1007/s10661-015-4690-4   AbstractWebsite

Size and growth rates for individual colonies are some of the most essential descriptive parameters for understanding coral communities, which are currently experiencing worldwide declines in health and extent. Accurately measuring coral colony size and changes over multiple years can reveal demographic, growth, or mortality patterns often not apparent from shortterm observations and can expose environmental stress responses that may take years to manifest. Describing community size structure can reveal population dynamics patterns, such as periods of failed recruitment or patterns of colony fission, which have implications for the future sustainability of these ecosystems. However, rapidly and non-invasively measuring coral colony sizes in situ remains a difficult task, as three-dimensional underwater digital reconstruction methods are currently not practical for large numbers of colonies. Twodimensional (2D) planar area measurements from projection of underwater photographs are a practical size proxy, although this method presents operational difficulties in obtaining well-controlled photographs in the highly rugose environment of the coral reef, and requires extensive time for image processing. Here, we present and test the measurement variance for a method of making rapid planar area estimates of small to medium-sized coral colonies using a lightweight monopod image-framing system and a custom semiautomated image segmentation analysis program. This method demonstrated a coefficient of variation of 2.26 % for repeated measurements in realistic ocean conditions, a level of error appropriate for rapid, inexpensive field studies of coral size structure, inferring change in colony size over time, or measuring bleaching or disease extent of large numbers of individual colonies.

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Georgiou, L, Falter J, Trotter J, Kline DI, Holcomb M, Dove SG, Hoegh-Guldberg O, McCulloch M.  2015.  pH homeostasis during coral calcification in a Free Ocean CO2 Enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef. . Proceedings of the National Academy of Sciences . 112(43):13219-13224.   10.1073/pnas.1505586112  
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Hamilton, TJ, Kline DI, Tresguerres M.  2018.  Shoaling behaviour is differentially altered by ethanol and dopamine D1 receptor modulators in tropical marine forage fish. Canadian Journal of Fisheries and Aquatic Sciences. (999):1-6.: NRC Research Press Abstract
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Kline, DI, Teneva L, Schneider K, Miard T, Chai A, Marker M, Headley K, Opdyke B, Nash M, Valetich M, Caves JK, Russell BD, Connell SD, Kirkwood BJ, Brewer P, Peltzer E, Silverman J, Caldeira K, Dunbar RB, Koseff JR, Monismith SG, Mitchell BG, Dove S, Hoegh-Guldberg O.  2012.  A short-term in situ CO2 enrichment experiment on Heron Island (GBR). Scientific Reports. 2   10.1038/srep00413   AbstractWebsite

Ocean acidification poses multiple challenges for coral reefs on molecular to ecological scales, yet previous experimental studies of the impact of projected CO2 concentrations have mostly been done in aquarium systems with corals removed from their natural ecosystem and placed under artificial light and seawater conditions. The Coral-Proto Free Ocean Carbon Enrichment System (CP-FOCE) uses a network of sensors to monitor conditions within each flume and maintain experimental pH as an offset from environmental pH using feedback control on the injection of low pH seawater. Carbonate chemistry conditions maintained in the -0.06 and -0.22 pH offset treatments were significantly different than environmental conditions. The results from this short-term experiment suggest that the CP-FOCE is an important new experimental system to study in situ impacts of ocean acidification on coral reef ecosystems.

Kline, DI, Teneva L, Hauri C, Schneider K, Miard T, Chai A, Marker M, Dunbar R, Caldeira K, Lazar B.  2015.  Six Month In Situ High-Resolution Carbonate Chemistry and Temperature Study on a Coral Reef Flat Reveals Asynchronous pH and Temperature Anomalies. PloS one. 10(6):e0127648.: Public Library of Science Abstract
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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.

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.

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Treibitz, T, Neal BP, Kline DI, Beijbom O, Roberts PLD, Mitchell BG, Kriegman D.  2015.  Wide field-of-view fluorescence imaging of coral reefs. Scientific Reports. 5   10.1038/srep07694   AbstractWebsite

Coral reefs globally are declining rapidly because of both local and global stressors. Improved monitoring tools are urgently needed to understand the changes that are occurring at appropriate temporal and spatial scales. Coral fluorescence imaging tools have the potential to improve both ecological and physiological assessments. Although fluorescence imaging is regularly used for laboratory studies of corals, it has not yet been used for large-scale in situ assessments. Current obstacles to effective underwater fluorescence surveying include limited field-of-view due to low camera sensitivity, the need for nighttime deployment because of ambient light contamination, and the need for custom multispectral narrow band imaging systems to separate the signal into meaningful fluorescence bands. Here we describe the Fluorescence Imaging System (FluorIS), based on a consumer camera modified for greatly increased sensitivity to chlorophyll-a fluorescence, and we show high spectral correlation between acquired images and in situ spectrometer measurements. This system greatly facilitates underwater wide field-of-view fluorophore surveying during both night and day, and potentially enables improvements in semi-automated segmentation of live corals in coral reef photographs and juvenile coral surveys.