Publications

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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
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.

2013
Reymond, CE, Lloyd A, Kline DI, Dove SG, Pandolfi JM.  2013.  Decline in growth of foraminifer Marginopora rossi under eutrophication and ocean acidification scenarios. Global Change Biology. 19:291-302.   10.1111/gcb.12035   AbstractWebsite

The combination of global and local stressors is leading to a decline in coral reef health globally. In the case of eutrophication, increased concentrations of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) are largely attributed to local land use changes. From the global perspective, increased atmospheric CO2 levels are not only contributing to global warming but also ocean acidification (OA). Both eutrophication and OA have serious implications for calcium carbonate production and dissolution among calcifying organisms. In particular, benthic foraminifera precipitate the most soluble form of mineral calcium carbonate (high-Mg calcite), potentially making them more sensitive to dissolution. In this study, a manipulative orthogonal two-factor experiment was conducted to test the effects of dissolved inorganic nutrients and OA on the growth, respiration and photophysiology of the large photosymbiont-bearing benthic foraminifer, Marginopora rossi. This study found the growth rate of M. rossi was inhibited by the interaction of eutrophication and acidification. The relationship between M. rossi and its photosymbionts became destabilized due to the photosymbiont's release from nutrient limitation in the nitrate-enriched treatment, as shown by an increase in zooxanthellae cells per host surface area. Foraminifers from the OA treatments had an increased amount of Chl a per cell, suggesting a greater potential to harvest light energy, however, there was no net benefit to the foraminifer growth. Overall, this study demonstrates that the impacts of OA and eutrophication are dose dependent and interactive. This research indicates an OA threshold at pH 7.6, alone or in combination with eutrophication, will lead to a decline in M. rossi calcification. The decline in foraminifera calcification associated with pollution and OA will have broad ecological implications across their ubiquitous range and suggests that without mitigation it could have serious implications for the future of coral reefs.

2012
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.

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.

Crawley, A, Kline DI, Dunn S, Anthony K, Dove S.  2010.  The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biology. 16:851-863.   10.1111/j.1365-2486.2009.01943.x   AbstractWebsite

Ocean acidification is expected to lower the net accretion of coral reefs yet little is known about its effect on coral photophysiology. This study investigated the effect of increasing CO(2) on photosynthetic capacity and photoprotection in Acropora formosa. The photoprotective role of photorespiration within dinoflagellates (genus Symbiodinium) has largely been overlooked due to focus on the presence of a carbon-concentrating mechanism despite the evolutionary persistence of a Form II Rubisco. The photorespiratory fixation of oxygen produces phosphoglycolate that would otherwise inhibit carbon fixation though the Calvin cycle if it were not converted to glycolate by phosphoglycolate phosphatase (PGPase). Glycolate is then either excreted or dealt with by enzymes in the photorespiratory glycolate and/or glycerate pathways adding to the pool of carbon fixed in photosynthesis. We found that CO(2) enrichment led to enhanced photoacclimation (increased chlorophyll a per cell) to the subsaturating light levels. Light-enhanced dark respiration per cell and xanthophyll de-epoxidation increased, with resultant decreases in photosynthetic capacity (P(nmax)) per chlorophyll. The conservative CO(2) emission scenario (A1B; 600-790 ppm) led to a 38% increase in the P(nmax) per cell whereas the 'business-as-usual' scenario (A1F1; 1160-1500 ppm) led to a 45% reduction in PGPase expression and no change in P(nmax) per cell. These findings support an important functional role for PGPase in dinoflagellates that is potentially compromised under CO(2) enrichment.