Publications

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2019
Fox, MD, Carter AL, Edwards CB, Takeshita Y, Johnson MD, Petrovic V, Amir CG, Sala E, Sandin SA, Smith JE.  2019.  Limited coral mortality following acute thermal stress and widespread bleaching on Palmyra Atoll, central Pacific. Coral Reefs. 38:701-712.   10.1007/s00338-019-01796-7   AbstractWebsite

During 2015-2016, an El Nino and associated warm water event caused widespread coral bleaching across the equatorial Pacific. Here, we combine 8 yr of benthic monitoring data from permanent photoquadrats with remotely sensed and in situ temperature measurements to assess the impact of the warming event on benthic communities at Palmyra Atoll. We quantified bleaching prevalence across two distinct reef habitats using the best available data. On the fore reef (similar to 10 m depth), we quantified bleaching severity within 100-200 m(2) large-area plots using the custom visualization and analysis software, Viscore. On the reef terrace (similar to 5 m depth), we used 95 focal colonies across three species that have been monitored annually since 2014. The 2015-2016 warm water event was the most extreme such event recorded on Palmyra in the past several decades with a maximum cumulative heat stress (degree heating weeks) of 11.9 degrees C-weeks. On the fore reef, 90% of live coral cover exhibited some degree of bleaching (32% severe bleaching). On the shallow reef terrace, bleaching was observed in 93% of the focal colonies across all species. Overall, coral cover declined 9% on the fore reef from 2014 to 2017, whereas coral cover did not change on the terrace. These contrasting results may be associated with typical daily temperature ranges on the terrace that are three times greater than on the fore reef. Permanent photoquadrats showed that turf algae initially colonized skeletons of recently dead corals but transitioned to crustose coralline algae within a year. Collectively, our study emphasizes that comprehensive monitoring of benthic communities over time combined with in situ temperature data can provide taxonomically precise trajectories of community change during and following thermal stress.

2018
d'Auriac, IG, Quinn RA, Maughan H, Nothias LF, Little M, Kapono CA, Cobian A, Reyes BT, Green K, Quistad SD, Leray M, Smith JE, Dorrestein PC, Rohwer F, Deheyn DD, Hartmann AC.  2018.  Before platelets: the production of platelet-activating factor during growth and stress in a basal marine organism. Proceedings of the Royal Society B-Biological Sciences. 285   10.1098/rspb.2018.1307   AbstractWebsite

Corals and humans represent two extremely disparate metazoan lineages and are therefore useful for comparative evolutionary studies. Two lipid-based molecules that are central to human immunity, platelet-activating factor (PAF) and Lyso-PAF were recently identified in scleractinian corals. To identify processes in corals that involve these molecules, PAF and Lyso-PAF biosynthesis was quantified in conditions known to stimulate PAF production in mammals (tissue growth and exposure to elevated levels of ultraviolet light) and in conditions unique to corals (competing with neighbouring colonies over benthic space). Similar to observations in mammals, PAF production was higher in regions of active tissue growth and increased when corals were exposed to elevated levels of ultraviolet light. PAF production also increased when corals were attacked by the stinging cells of a neighbouring colony, though only the attacked coral exhibited an increase in PAF. This reaction was observed in adjacent areas of the colony, indicating that this response is coordinated across multiple polyps including those not directly subject to the stress. PAF and Lyso-PAF are involved in coral stress responses that are both shared with mammals and unique to the ecology of cnidarians.

2017
Furby, KA, Smith JE, Sandin SA.  2017.  Porites superfusa mortality and recovery from a bleaching event at Palmyra Atoll USA. Peerj. 5   10.7717/peerj.3204   AbstractWebsite

Background. The demography of a coral colony is not a binary trajectory of life and death. Based on the flexibility afforded by colonial organization, most reef-building corals employ a variety of dynamic survival strategies, including growth and shrinkage. The demographic flexibility affects coral size, shape and reproductive output, among other factors. It is thus critical to quantify the relative importance of key dynamics of recruitment, mortality, growth and shrinkage in changing the overall cover of coral on a reef. Methods. Using fixed photographic quadrats, we tracked the patterns of change in the cover of one common central Pacific coral, Porites superfusa, before and after the 2009 ENSO event. Results. Coral colonies suffered both whole and partial colony mortality, although larger colonies were more likely to survive. In subsequent years, recruitment of new colonies and regrowth of surviving colonies both contributed to the modest recovery of P. superfusa. Discussion. This study is unique in its quantitative comparisons of coral recruitment versus regrowth during periods of areal expansion. Our data suggest that recovery is not limited simply to the long pathway of settlement, recruitment and early growth of new colonies but is accelerated by means of regrowth of already established colonies having suffered partial mortality.

2015
Haas, AF, Guibert M, Foerschner A, Co T, Calhoun S, George E, Hatay M, Dinsdale E, Sandin SA, Smith JE, Vermeij MJA, Felts B, Dustan P, Salamon P, Rohwer F.  2015.  Can we measure beauty? Computational evaluation of coral reef aesthetics Peerj. 3   10.7717/peerj.1390   AbstractWebsite

The natural beauty of coral reefs attracts millions of tourists worldwide resulting in substantial revenues for the adjoining economies. Although their visual appearance is a pivotal factor attracting humans to coral reefs current monitoring protocols exclusively target biogeochemical parameters, neglecting changes in their aesthetic appearance. Here we introduce a standardized computational approach to assess coral reef environments based on 109 visual features designed to evaluate the aesthetic appearance of art. The main feature groups include color intensity and diversity of the image, relative size, color, and distribution of discernable objects within the image, and texture. Specific coral reef aesthetic values combining all 109 features were calibrated against an established biogeochemical assessment (NCEAS) using machine learning algorithms. These values were generated for similar to 2,100 random photographic images collected from 9 coral reef locations exposed to varying levels of anthropogenic influence across 2 ocean systems. Aesthetic values proved accurate predictors of the NCEAS scores (root mean square error <5 for N >= 3) and significantly correlated to microbial abundance at each site. This shows that mathematical approaches designed to assess the aesthetic appearance of photographic images can be used as an inexpensive monitoring tool for coral reef ecosystems. It further suggests that human perception of aesthetics is not purely subjective but influenced by inherent reactions towards measurable visual cues. By quantifying aesthetic features of coral reef systems this method provides a cost efficient monitoring tool that targets one of the most important socioeconomic values of coral reefs directly tied to revenue for its local population.

2014
Williams, GJ, Price NN, Ushijima B, Aeby GS, Callahan S, Davy SK, Gove JM, Johnson MD, Knapp IS, Shore-Maggio A, Smith JE, Videau P, Work TM.  2014.  Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease. Proceedings of the Royal Society B-Biological Sciences. 281   10.1098/rspb.2013.3069   AbstractWebsite

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.

2013
Nelson, CE, Goldberg SJ, Kelly LW, Haas AF, Smith JE, Rohwer F, Carlson CA.  2013.  Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. Isme Journal. 7:962-979.   10.1038/ismej.2012.161   AbstractWebsite

Increasing algal cover on tropical reefs worldwide may be maintained through feedbacks whereby algae outcompete coral by altering microbial activity. We hypothesized that algae and coral release compositionally distinct exudates that differentially alter bacterioplankton growth and community structure. We collected exudates from the dominant hermatypic coral holobiont Porites spp. and three dominant macroalgae (one each Ochrophyta, Rhodophyta and Chlorophyta) from reefs of Mo'orea, French Polynesia. We characterized exudates by measuring dissolved organic carbon (DOC) and fractional dissolved combined neutral sugars (DCNSs) and subsequently tracked bacterioplankton responses to each exudate over 48 h, assessing cellular growth, DOC/DCNS utilization and changes in taxonomic composition (via 16S rRNA amplicon pyrosequencing). Fleshy macroalgal exudates were enriched in the DCNS components fucose (Ochrophyta) and galactose (Rhodophyta); coral and calcareous algal exudates were enriched in total DCNS but in the same component proportions as ambient seawater. Rates of bacterioplankton growth and DOC utilization were significantly higher in algal exudate treatments than in coral exudate and control incubations with each community selectively removing different DCNS components. Coral exudates engendered the smallest shift in overall bacterioplankton community structure, maintained high diversity and enriched taxa from Alphaproteobacteria lineages containing cultured representatives with relatively few virulence factors (VFs) (Hyphomonadaceae and Erythrobacteraceae). In contrast, macroalgal exudates selected for less diverse communities heavily enriched in copiotrophic Gammaproteobacteria lineages containing cultured pathogens with increased VFs (Vibrionaceae and Pseudoalteromonadaceae). Our results demonstrate that algal exudates are enriched in DCNS components, foster rapid growth of bacterioplankton and select for bacterial populations with more potential VFs than coral exudates. The ISME Journal (2013) 7, 962-979; doi:10.1038/ismej.2012.161; published online 10 January 2013

2011
Price, NN, Hamilton SL, Tootell JS, Smith JE.  2011.  Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Marine Ecology-Progress Series. 440:67-78.   10.3354/meps09309   AbstractWebsite

Ocean acidification (OA), resulting from increasing dissolved carbon dioxide (CO(2)) in surface waters, is likely to affect many marine organisms, particularly those that calcify. Recent OA studies have demonstrated negative and/or differential effects of reduced pH on growth, development, calcification and physiology, but most of these have focused on taxa other than calcareous benthic macroalgae. Here we investigate the potential effects of OA on one of the most common coral reef macroalgal genera, Halimeda. Species of Halimeda produce a large proportion of the sand in the tropics and are a major contributor to framework development on reefs because of their rapid calcium carbonate production and high turnover rates. On Palmyra Atoll in the central Pacific, we conducted a manipulative bubbling experiment to investigate the potential effects of OA on growth, calcification and photophysiology of 2 species of Halimeda. Our results suggest that Halimeda is highly susceptible to reduced pH and aragonite saturation state but the magnitude of these effects is species specific. H. opuntia suffered net dissolution and 15% reduction in photosynthetic capacity, while H. taenicola did not calcify but did not alter photophysiology in experimental treatments. The disparate responses of these species to elevated CO(2) partial pressure (pCO(2)) may be due to anatomical and physiological differences and could represent a shift in their relative dominance in the face of OA. The ability for a species to exert biological control over calcification and the species specific role of the carbonate skeleton may have important implications for the potential effects of OA on ecological function in the future.

2006
Smith, JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL.  2006.  Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecology Letters. 9:835-845.   10.1111/j.1461-0248.2006.00937.x   AbstractWebsite

Declines in coral cover are generally associated with increases in the abundance of fleshy algae. In many cases, it remains unclear whether algae are responsible, directly or indirectly, for coral death or whether they simply settle on dead coral surfaces. Here, we show that algae can indirectly cause coral mortality by enhancing microbial activity via the release of dissolved compounds. When coral and algae were placed in chambers together but separated by a 0.02 mu m filter, corals suffered 100% mortality. With the addition of the broad-spectrum antibiotic ampicillin, mortality was completely prevented. Physiological measurements showed complementary patterns of increasing coral stress with proximity to algae. Our results suggest that as human impacts increase and algae become more abundant on reefs a positive feedback loop may be created whereby compounds released by algae enhance microbial activity on live coral surfaces causing mortality of corals and further algal growth.