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2016
Kelly, ELA, Eynaud Y, Clements SM, Gleason M, Sparks RT, Williams ID, Smith JE.  2016.  Investigating functional redundancy versus complementarity in Hawaiian herbivorous coral reef fishes. Oecologia. 182:1151-1163.   10.1007/s00442-016-3724-0   AbstractWebsite

Patterns of species resource use provide insight into the functional roles of species and thus their ecological significance within a community. The functional role of herbivorous fishes on coral reefs has been defined through a variety of methods, but from a grazing perspective, less is known about the species-specific preferences of herbivores on different groups of reef algae and the extent of dietary overlap across an herbivore community. Here, we quantified patterns of redundancy and complementarity in a highly diverse community of herbivores at a reef on Maui, Hawaii, USA. First, we tracked fish foraging behavior in situ to record bite rate and type of substrate bitten. Second, we examined gut contents of select herbivorous fishes to determine consumption at a finer scale. Finally, we placed foraging behavior in the context of resource availability to determine how fish selected substrate type. All species predominantly (73-100 %) foraged on turf algae, though there were differences among the types of macroalgae and other substrates bitten. Increased resolution via gut content analysis showed the composition of turf algae consumed by fishes differed across herbivore species. Consideration of foraging behavior by substrate availability revealed 50 % of herbivores selected for turf as opposed to other substrate types, but overall, there were variable foraging portfolios across all species. Through these three methods of investigation, we found higher complementarity among herbivorous fishes than would be revealed using a single metric. These results suggest differences across species in the herbivore "rain of bites" that graze and shape benthic community composition.

Takeshita, Y, McGillis W, Briggs EM, Carter AL, Donham EM, Martz TR, Price NN, Smith JE.  2016.  Assessment of net community production and calcification of a coral reef using a boundary layer approach. Journal of Geophysical Research-Oceans. 121:5655-5671.   10.1002/2016jc011886   AbstractWebsite

Coral reefs are threatened worldwide, and there is a need to develop new approaches to monitor reef health under natural conditions. Because simultaneous measurements of net community production (NCP) and net community calcification (NCC) are used as important indicators of reef health, tools are needed to assess them in situ. Here we present the Benthic Ecosystem and Acidification Measurement System (BEAMS) to provide the first fully autonomous approach capable of sustained, simultaneous measurements of reef NCP and NCC under undisturbed, natural conditions on time scales ranging from tens of minutes to weeks. BEAMS combines the chemical and velocity gradient in the benthic boundary layer to quantify flux from the benthos for a variety of parameters to measure NCP and NCC. Here BEAMS was used to measure these rates from two different sites with different benthic communities on the western reef terrace at Palmyra Atoll for 2 weeks in September 2014. Measurements were made every similar to 15 min. The trends in metabolic rates were consistent with the benthic communities between the two sites with one dominated by fleshy organisms and the other dominated by calcifiers (degraded and healthy reefs, respectively). This demonstrates the potential utility of BEAMS as a reef health monitoring tool. NCP and NCC were tightly coupled on time scales of minutes to days, and light was the primary driver for the variability of daily integrated metabolic rates. No correlation between CO2 levels and daily integrated NCC was observed, indicating that NCC at these sites were not significantly affected by CO2.

Mullen, AD, Treibitz T, Roberts PLD, Kelly ELA, Horwitz R, Smith JE, Jaffe JS.  2016.  Underwater microscopy for in situ studies of benthic ecosystems. Nature Communications. 7: Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.   10.1038/ncomms12093   Abstract

Microscopic-scale processes significantly influence benthic marine ecosystems such as coral reefs and kelp forests. Due to the ocean/'s complex and dynamic nature, it is most informative to study these processes in the natural environment yet it is inherently difficult. Here we present a system capable of non-invasively imaging seafloor environments and organisms in situ at nearly micrometre resolution. We overcome the challenges of underwater microscopy through the use of a long working distance microscopic objective, an electrically tunable lens and focused reflectance illumination. The diver-deployed instrument permits studies of both spatial and temporal processes such as the algal colonization and overgrowth of bleaching corals, as well as coral polyp behaviour and interspecific competition. By enabling in situ observations at previously unattainable scales, this instrument can provide important new insights into micro-scale processes in benthic ecosystems that shape observed patterns at much larger scales.

Kaplanis, NJ, Harris JL, Smith JE.  2016.  Distribution patterns of the non-native seaweeds Sargassum horneri (Turner) C. Agardh and Undaria pinnatifida (Harvey) Suringar on the San Diego and Pacific coast of North America. Aquatic Invasions. 11:111-124.   10.3391/ai.2016.11.2.01   AbstractWebsite

Here we report the occurrence of the two non-native brown macroalgal species Sargassum horneri (Turner) C. Agardh and Undaria pinnatifida (Harvey) Suringar in San Diego County and describe expansions in their ranges and new invasions on the California and Baja California coasts. Both species have exhibited characteristics of successful invaders: establishing in new areas, spreading locally, and persisting through multiple generations in areas that have been invaded. These species now occur primarily in harbors, but have also invaded open coast sites, suggesting that they can invade areas with relatively high wave action and with well-established native benthic communities. The rapid and uncontrolled spread of these species to date has serious implications for their expansion along the west coast of North America. The ecological and economic consequences of these invasions require further research.

Haas, AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA, Giles S, Hatay M, Hisakawa N, Knowles B, Lim YW, Maughan H, Pantos O, Roach TNF, Sanchez SE, Silveira CB, Sandin S, Smith JE, Rohwer F.  2016.  Global microbialization of coral reefs. Nature Microbiology. 1   10.1038/nmicrobiol.2016.42   AbstractWebsite

Microbialization refers to the observed shift in ecosystem trophic structure towards higher microbial biomass and energy use. On coral reefs, the proximal causes of microbialization are overfishing and eutrophication, both of which facilitate enhanced growth of fleshy algae, conferring a competitive advantage over calcifying corals and coralline algae. The proposed mechanism for this competitive advantage is the DDAM positive feedback loop (dissolved organic carbon (DOC), disease, algae, microorganism), where DOC released by ungrazed fleshy algae supports copiotrophic, potentially pathogenic bacterial communities, ultimately harming corals and maintaining algal competitive dominance. Using an unprecedented data set of >400 samples from 60 coral reef sites, we show that the central DDAM predictions are consistent across three ocean basins. Reef algal cover is positively correlated with lower concentrations of DOC and higher microbial abundances. On turf and fleshy macroalgal-rich reefs, higher relative abundances of copiotrophic microbial taxa were identified. These microbial communities shift their metabolic potential for carbohydrate degradation from the more energy efficient Embden-Meyerhof-Parnas pathway on coral-dominated reefs to the less efficient Entner-Doudoroff and pentose phosphate pathways on algal-dominated reefs. This 'yield-to-power' switch by microorganism directly threatens reefs via increased hypoxia and greater CO2 release from the microbial respiration of DOC.

Quinn, RA, Vermeij MJA, Hartmann AC, d'Auriac IG, Benler S, Haas A, Quistad SD, Lim YW, Little M, Sandin S, Smith JE, Dorrestein PC, Rohwer F.  2016.  Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence. Proceedings of the Royal Society B-Biological Sciences. 283   10.1098/rspb.2016.0469   AbstractWebsite

Holobionts are assemblages of microbial symbionts and their macrobial host. As extant representatives of some of the oldest macro-organisms, corals and algae are important for understanding how holobionts develop and interact with one another. Using untargeted metabolomics, we show that non-self interactions altered the coral metabolome more than self-interactions (i.e. different or same genus, respectively). Platelet activating factor (PAF) and Lyso-PAF, central inflammatory modulators in mammals, were major lipid components of the coral holobionts. When corals were damaged during competitive interactions with algae, PAF increased along with expression of the gene encoding Lyso-PAF acetyltransferase; the protein responsible for converting Lyso-PAF to PAF. This shows that self and non-self recognition among some of the oldest extant holobionts involve bioactive lipids identical to those in highly derived taxa like humans. This further strengthens the hypothesis that major players of the immune response evolved during the pre-Cambrian.

Knowles, B, Silveira CB, Bailey BA, Barott K, Cantu VA, Cobian-Guemes AG, Coutinho FH, Dinsdale EA, Felts B, Furby KA, George EE, Green KT, Gregoracci GB, Haas AF, Haggerty JM, Hester ER, Hisakawa N, Kelly LW, Lim YW, Little M, Luque A, McDole-Somera T, McNair K, de Oliveira LS, Quistad SD, Robinett NL, Sala E, Salamon P, Sanchez SE, Sandin S, Silva GGZ, Smith J, Sullivan C, Thompson C, Vermeij MJA, Youle M, Young C, Zgliczynski B, Brainard R, Edwards RA, Nulton J, Thompson F, Rohwer F.  2016.  Lytic to temperate switching of viral communities. Nature. 531:466-+.   10.1038/nature17193   AbstractWebsite

Microbial viruses can control host abundances via density-dependent lytic predator-prey dynamics. Less clear is how temperate viruses, which coexist and replicate with their host, influence microbial communities. Here we show that virus-like particles are relatively less abundant at high host densities. This suggests suppressed lysis where established models predict lytic dynamics are favoured. Meta-analysis of published viral and microbial densities showed that this trend was widespread in diverse ecosystems ranging from soil to freshwater to human lungs. Experimental manipulations showed viral densities more consistent with temperate than lytic life cycles at increasing microbial abundance. An analysis of 24 coral reef viromes showed a relative increase in the abundance of hallmark genes encoded by temperate viruses with increased microbial abundance. Based on these four lines of evidence, we propose the Piggyback-the-Winner model wherein temperate dynamics become increasingly important in ecosystems with high microbial densities; thus 'more microbes, fewer viruses'.

Smith, JE, Brainard R, Carter A, Grillo S, Edwards C, Harris J, Lewis L, Obura D, Rohwer F, Sala E, Vroom PS, Sandin S.  2016.  Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proceedings of the Royal Society B-Biological Sciences. 283   10.1098/rspb.2015.1985   AbstractWebsite

Numerous studies have documented declines in the abundance of reef-building corals over the last several decades and in some but not all cases, phase shifts to dominance by macroalgae have occurred. These assessments, however, often ignore the remainder of the benthos and thus provide limited information on the present-day structure and function of coral reef communities. Here, using an unprecedentedly large dataset collected within the last 10 years across 56 islands spanning five archipelagos in the central Pacific, we examine how benthic reef communities differ in the presence and absence of human populations. Using islands as replicates, we examine whether benthic community structure is associated with human habitation within and among archipelagos and across latitude. While there was no evidence for coral to macroalgal phase shifts across our dataset we did find that the majority of reefs on inhabited islands were dominated by fleshy non-reef-building organisms (turf algae, fleshy macroalgae and non-calcifying invertebrates). By contrast, benthic communities from uninhabited islands were more variable but in general supported more calcifiers and active reef builders (stony corals and crustose coralline algae). Our results suggest that cumulative human impacts across the central Pacific may be causing a reduction in the abundance of reef builders resulting in island scale phase shifts to dominance by fleshy organisms.

2015
Vargas-Angel, B, Richards CL, Vroom PS, Price NN, Schils T, Young CW, Smith J, Johnson MD, Brainard RE.  2015.  Baseline assessment of net calcium carbonate accretion rates on US Pacific reefs. Plos One. 10   10.1371/journal.pone.0142196   AbstractWebsite

This paper presents a comprehensive quantitative baseline assessment of in situ net calcium carbonate accretion rates (g CaCO3 cm(-2) yr(-1)) of early successional recruitment communities on Calcification Accretion Unit (CAU) plates deployed on coral reefs at 78 discrete sites, across 11 islands in the central and south Pacific Oceans. Accretion rates varied substantially within and between islands, reef zones, levels of wave exposure, and island geomorphology. For forereef sites, mean accretion rates were the highest at Rose Atoll, Jarvis, and Swains Islands, and the lowest at Johnston Atoll and Tutuila. A comparison between reef zones showed higher accretion rates on forereefs compared to lagoon sites; mean accretion rates were also higher on windward than leeward sites but only for a subset of islands. High levels of spatial variability in net carbonate accretion rates reported herein draw attention to the heterogeneity of the community assemblages. Percent cover of key early successional taxa on CAU plates did not reflect that of the mature communities present on surrounding benthos, possibly due to the short deployment period (2 years) of the experimental units. Yet, net CaCO3 accretion rates were positively correlated with crustose coralline algae (CCA) percent cover on the surrounding benthos and on the CAU plates, which on average represented >70% of the accreted material. For foreeefs and lagoon sites combined CaCO3 accretion rates were statistically correlated with total alkalinity and Chlorophyll-a; a GAM analysis indicated that SiOH and Halimeda were the best predictor variables of accretion rates on lagoon sites, and total alkalinity and Chlorophyll-a for forereef sites, demonstrating the utility of CAUs as a tool to monitor changes in reef accretion rates as they relate to ocean acidification. This study underscores the pivotal role CCA play as a key benthic component and supporting actively calcifying reefs; high Mg-calcite exoskeletons makes CCA extremely susceptible changes in ocean water pH, emphasizing the far-reaching threat that ocean acidification poses to the ecological function and persistence of coral reefs worldwide.

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.

Takeshita, Y, Frieder CA, Martz TR, Ballard JR, Feely RA, Kram S, Nam S, Navarro MO, Price NN, Smith JE.  2015.  Including high-frequency variability in coastal ocean acidification projections. Biogeosciences. 12:5853-5870.   10.5194/bg-12-5853-2015   AbstractWebsite

Assessing the impacts of anthropogenic ocean acidification requires knowledge of present-day and future environmental conditions. Here, we present a simple model for upwelling margins that projects anthropogenic acidification trajectories by combining high-temporal-resolution sensor data, hydrographic surveys for source water characterization, empirical relationships of the CO2 system, and the atmospheric CO2 record. This model characterizes CO2 variability on timescales ranging from hours (e. g., tidal) to months (e. g., seasonal), bridging a critical knowledge gap in ocean acidification research. The amount of anthropogenic carbon in a given water mass is dependent on the age; therefore a density-age relationship was derived for the study region and then combined with the 2013 Intergovernmental Panel on Climate Change CO2 emission scenarios to add density-dependent anthropogenic carbon to the sensor time series. The model was applied to time series from autonomous pH sensors deployed in the surf zone, kelp forest, submarine canyon edge, and shelf break in the upper 100m of the Southern California Bight. All habitats were within 5 km of one another, and exhibited unique, habitat-specific CO2 variability signatures and acidification trajectories, demonstrating the importance of making projections in the context of habitat-specific CO2 signatures. In general, both the mean and range of pCO(2) increase in the future, with the greatest increase in both magnitude and range occurring in the deeper habitats due to reduced buffering capacity. On the other hand, the saturation state of aragonite (Omega(Ar)) decreased in both magnitude and range. This approach can be applied to the entire California Current System, and upwelling margins in general, where sensor and complementary hydrographic data are available.

Harris, JL, Lewis LS, Smith JE.  2015.  Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Marine Ecology Progress Series. 532:41-57.   10.3354/meps11344   AbstractWebsite

Quantifying variability over multiple spatial scales is a fundamental goal in ecology, providing insight into which scale-dependent processes most strongly influence community structure. On coral reefs, the ubiquitous turf algae are the primary food source for herbivores and competitors for space with corals. Turf algae will likely increase in the future, because they thrive under conditions that reduce coral cover. Turfs are typically treated as a single homogeneous functional group, but analyzing them as a variable assemblage is more informative. We used a hierarchical sampling design to quantify 4 scales of variability in turf assemblages from centimeters (within single dead coral heads) to kilometers (across islands) on the rarely studied Lhaviyani Atoll, Maldives. We used 4 metrics, each reflecting different ecological processes: percent cover, canopy height, richness, and assemblage composition. For most of these metrics, variability was significant at multiple spatial scales. However, for all metrics, the smallest scale (centimeters) explained the greatest proportion of overall variability. The least variability in cover, canopy height, and richness occurred among sites (100s meters), suggesting that processes such as competition, predation, and vegetative growth are heterogeneous at small scales. In contrast, assemblage composition was least variable at the largest scale (kilometers), suggesting that oceanographic processes or a well-mixed propagule supply reduce variability. With declining coral and increasing cover of turf on reefs worldwide, it will become increasingly important to understand the dynamics of coral-turf competitive interactions. However, because turf assemblages are highly variable at small spatial scales, these interactions require more detailed consideration.

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.

Bracken, MES, Hillebrand H, Borer ET, Seabloom EW, Cebrian J, Cleland EE, Elser JJ, Gruner DS, Harpole WS, Ngai JT, Smith JE.  2015.  Signatures of nutrient limitation and co-limitation: responses of autotroph internal nutrient concentrations to nitrogen and phosphorus additions. Oikos. 124:113-121.   10.1111/oik.01215   AbstractWebsite

Humans are modifying the availability of nutrients such as nitrogen (N) and phosphorus (P), and it is therefore important to understand how these nutrients, independently or in combination, influence the growth and nutrient content of primary producers. Using meta-analysis of 118 field and laboratory experiments in freshwater, marine and terrestrial ecosystems, we tested hypotheses about co-limitation of N and P by comparing the effects of adding N alone, P alone, and both N and P together on internal N (e.g. %N, C:N) and P (e.g. %P, C:P) concentrations in autotroph communities. In particular, we tested the following predictions. First, if only one nutrient was limiting, addition of that nutrient should decrease the concentration of the other nutrient, but addition of the non-limiting nutrient would have no effect on the internal concentration of the limiting nutrient. If community co-limitation was occurring then addition of either nutrient should result in a decrease in the internal concentration of the other nutrient. Community co-limitation could also result in no change - or even an increase - in N concentrations in response to P addition if P stimulated growth of N fixers. Finally, if biochemically dependent co-limitation was occurring, addition of a limiting nutrient would not decrease, and could even increase, the concentration of the other, co-limited nutrient. We found no general evidence for the decrease in the internal concentration of one nutrient due to addition of another nutrient. The one exception to this overall pattern was marine systems, where N addition decreased internal P concentrations. In contrast, P addition increased internal N concentrations across all experiments, consistent with co-limitation. These results have important implications for understanding the roles that N and P play in controlling producer growth and internal nutrient accumulation as well as for managing the effects of nutrient enrichment in ecosystems. Synthesis On a global scale, humans have doubled nitrogen (N) inputs and quadrupled phosphorus (P) inputs relative to pre-industrial levels. N and P fertilization influences autotroph internal nutrient concentrations and ratios and thereby affects a variety of community and ecosystem processes, including decomposition and consumer population dynamics. It is therefore critical to understand the effects of nutrient additions on the growth and nutrient concentrations of primary producers. We used meta-analysis to evaluate the responses of autotroph internal N and P concentrations to additions of N, P, and N+P and make inferences about limitation and co-limitation of N and P across marine, terrestrial, and freshwater ecosystems. We found little evidence for single-nutrient limitation, highlighting the fact that multiple nutrients generally limit primary production.

2014
Lim, YW, Cuevas DA, Silva GGZ, Aguinaldo K, Dinsdale EA, Haas AF, Hatay M, Sanchez SE, Wegley-Kelly L, Dutilh BE, Harkins TT, Lee CC, Tom W, Sandin SA, Smith JE, Zgliczynski B, Vermeij MJA, Rohwer F, Edwards RA.  2014.  Sequencing at sea: challenges and experiences in Ion Torrent PGM sequencing during the 2013 Southern Line Islands Research Expedition. Peerj. 2   10.7717/peerj.520   AbstractWebsite

Genomics and metagenomics have revolutionized our understanding of marine microbial ecology and the importance of microbes in global geochemical cycles. However, the process of DNA sequencing has always been an abstract extension of the research expedition, completed once the samples were returned to the laboratory. During the 2013 Southern Line Islands Research Expedition, we started the first effort to bring next generation sequencing to some of the most remote locations on our planet. We successfully sequenced twenty six marine microbial genomes, and two marine microbial metagenomes using the Ion Torrent PGM platform on the Merchant Yacht Hanse Explorer. Onboard sequence assembly, annotation, and analysis enabled us to investigate the role of the microbes in the coral reef ecology of these islands and atolls. This analysis identified phosphonate as an important phosphorous source for microbes growing in the Line Islands and reinforced the importance of L-serine in marine microbial ecosystems. Sequencing in the field allowed us to propose hypotheses and conduct experiments and further sampling based on the sequences generated. By eliminating the delay between sampling and sequencing, we enhanced the productivity of the research expedition. By overcoming the hurdles associated with sequencing on a boat in the middle of the Pacific Ocean we proved the flexibility of the sequencing, annotation, and analysis pipelines.

Kelly, LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA, Haas AF, Haynes M, Lim YW, McDole T, Nelson CE, Sala E, Sandin SA, Smith JE, Vermeij MJA, Youle M, Rohwer F.  2014.  Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proceedings of the National Academy of Sciences of the United States of America. 111:10227-10232.   10.1073/pnas.1403319111   AbstractWebsite

Holobionts are species-specific associations between macro-and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e. g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e. g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.

Johnson, MD, Price NN, Smith JE.  2014.  Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. Peerj. 2   10.7717/peerj.411   AbstractWebsite

Despite the heightened awareness of ocean acidification (OA) effects on marine organisms, few studies empirically juxtapose biological responses to CO2 manipulations across functionally distinct primary producers, particularly benthic algae. Algal responses to OA may vary because increasing CO2 has the potential to fertilize photosynthesis but impair biomineralization. Using a series of repeated experiments on Palmyra Atoll, simulated OA effects were tested across a suite of ecologically important coral reef algae, including five fleshy and six calcareous species. Growth, calcification and photophysiology were measured for each species independently and metrics were combined from each experiment using a meta-analysis to examine overall trends across functional groups categorized as fleshy, upright calcareous, and crustose coralline algae (CCA). The magnitude of the effect of OA on algal growth response varied by species, but the direction was consistent within functional groups. Exposure to OA conditions generally enhanced growth in fleshy macroalgae, reduced net calcification in upright calcareous algae, and caused net dissolution in CCA. Additionally, three of the five fleshy seaweeds tested became reproductive upon exposure to OA conditions. There was no consistent effect of OA on algal photophysiology. Our study provides experimental evidence to support the hypothesis that OA will reduce the ability of calcareous algae to biomineralize. Further, we show that CO2 enrichment either will stimulate population or somatic growth in some species of fleshy macroalgae. Thus, our results suggest that projected OA conditions may favor non-calcifying algae and influence the relative dominance of fleshy macroalgae on reefs, perpetuating or exacerbating existing shifts in reef community structure.

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.

Hamilton, SL, Smith JE, Price NN, Sandin SA.  2014.  Quantifying patterns of fish herbivory on Palmyra Atoll (USA), an uninhabited predator-dominated central Pacific coral reef. Marine Ecology Progress Series. 501:141-155.   10.3354/meps10684   AbstractWebsite

On many coral reefs, herbivorous fish play an essential role in regulating algal growth and influencing the outcome of coral-algal competition. Working on a remote predator-dominated coral reef on Palmyra Atoll, USA, we used behavioral foraging observations to quantify the roles of common parrotfish and surgeonfish in the roving herbivore guild. We recorded species-specific bite rates on different benthic organisms, quantified the relative abundance of those benthic organisms, and estimated benthos-specific grazing intensities as a function of bite rates, fish abundance, and percent cover. These grazing metrics were compared between the exposed fore reef (similar to 10 m depth) and protected reef terrace (similar to 5 m depth) habitats. We observed large differences in feeding rates and substrate selectivity among fish species. Most species fed predominately on algal turfs; however, some species foraged broadly among fleshy macroalgal taxa, while others specialized on calcified green algae of the genus Halimeda. The highest bite rates were recorded from species targeting algal turfs, while the highest rates of defecation were recorded from species targeting Halimeda. Per capita bite rates of all species were higher in the fore reef habitat (mean 45% more bites min(-1)); however, overall grazing intensities on turf algae (bites cm(-2) d(-1)) were 5 times higher on the reef terrace than on the fore reef. Despite habitat-specific differences in the herbivore assemblages, the estimated distribution of total bites showed consistency among habitats, with strong guild-level positive foraging selectivity for algal turf. Comparisons of bite and defecation rate data for these herbivores across the Indo-Pacific highlight phylogenetic constraints on grazing activities. Overall, this study illustrates the importance of herbivore functional redundancy, variability in species-specific grazing, and provides a framework for assessing guild-wide grazing impacts on coral reefs.

Edwards, CB, Friedlander AM, Green AG, Hardt MJ, Sala E, Sweatman HP, Williams ID, Zgliczynski B, Sandin SA, Smith JE.  2014.  Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proceedings of the Royal Society B-Biological Sciences. 281   10.1098/rspb.2013.1835   AbstractWebsite

On coral reefs, herbivorous fishes consume benthic primary producers and regulate competition between fleshy algae and reef-building corals. Many of these species are also important fishery targets, yet little is known about their global status. Using a large-scale synthesis of peer-reviewed and unpublished data, we examine variability in abundance and biomass of herbivorous reef fishes and explore evidence for fishing impacts globally and within regions. We show that biomass is more than twice as high in locations not accessible to fisheries relative to fisheries-accessible locations. Although there are large biogeographic differences in total biomass, the effects of fishing are consistent in nearly all regions. We also show that exposure to fishing alters the structure of the herbivore community by disproportionately reducing biomass of large-bodied functional groups (scraper/excavators, browsers, grazer/detritivores), while increasing biomass and abundance of territorial algal-farming damselfishes (Pomacentridae). The browser functional group that consumes macroalgae and can help to prevent coral-macroalgal phase shifts appears to be most susceptible to fishing. This fishing down the herbivore guild probably alters the effectiveness of these fishes in regulating algal abundance on reefs. Finally, data from remote and unfished locations provide important baselines for setting management and conservation targets for this important group of fishes.

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

McLeod, E, Anthony KRN, Andersson A, Beeden R, Golbuu Y, Kleypas J, Kroeker K, Manzello D, Salm RV, Schuttenberg H, Smith JE.  2013.  Preparing to manage coral reefs for ocean acidification: lessons from coral bleaching. Frontiers in Ecology and the Environment. 11:20-27.   10.1890/110240   AbstractWebsite

Ocean acidification is a direct consequence of increasing atmospheric carbon dioxide concentrations and is expected to compromise the structure and function of coral reefs within this century. Research into the effects of ocean acidification on coral reefs has focused primarily on measuring and predicting changes in seawater carbon (C) chemistry and the biological and geochemical responses of reef organisms to such changes. To date, few ocean acidification studies have been designed to address conservation planning and management priorities. Here, we discuss how existing marine protected area design principles developed to address coral bleaching may be modified to address ocean acidification. We also identify five research priorities needed to incorporate ocean acidification into conservation planning and management: (1) establishing an ocean C chemistry baseline, (2) establishing ecological baselines, (3) determining species/habitat/community sensitivity to ocean acidification, (4) projecting changes in seawater carbonate chemistry, and (5) identifying potentially synergistic effects of multiple stressors.

Smith, JE, Price NN, Nelson CE, Haas AF.  2013.  Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Marine Biology. 160:2437-2447.   10.1007/s00227-013-2239-z   AbstractWebsite

Benthic marine primary producers affect the chemistry of their surrounding environment through metabolic processes. Photosynthesis and respiration will elevate or depress the concentration of oxygen in the diffusive boundary layer. Likewise, acid-base regulation and biomineralization/dissolution for calcifying species can alter the relative concentration of inorganic carbon species and thus pH. Here, we measured the relative ability of several common benthic primary producers from coral reef systems of the central Pacific and the Caribbean to simultaneously affect seawater oxygen concentration and pH values. Repeated measurements over a diel cycle confirmed that several primary producers substantially alter surrounding seawater chemistry over time. The majority of fleshy algae exhibited a stoichiometric ratio of oxygen to hydrogen ions not significantly different from one during daylight hours. In contrast, calcifiers exhibited significantly lower oxygen to hydrogen ion ratios that were unique for each species and were inversely correlated with known rates of calcification. These data provide the first quantitative estimates of the simultaneous influence of several species of benthic primary producers on water column oxygen concentrations and pH across different tropical reef systems. Finally, because more productive fleshy taxa have the potential to raise both oxygen and pH during the day to a greater extent than calcified species, our results suggest that some fleshy taxa may provide a buffering capacity to future ocean acidification scenarios.

Vermeij, MJA, van der Heijden RA, Olthuis JG, Marhaver KL, Smith JE, Visser PM.  2013.  Survival and dispersal of turf algae and macroalgae consumed by herbivorous coral reef fishes. Oecologia. 171:417-425.: Springer-Verlag   10.1007/s00442-012-2436-3   AbstractWebsite

The mechanisms by which algae disperse across space on coral reefs are poorly known. We investigated the ability of four common Caribbean herbivorous fish species to disperse viable algal fragments through consumption of macroalgae and subsequent defecation. Fragments of all major algal taxa (Phaeophyta, Rhodophyta, and Chlorophyta) were found in 98.7 % of the fecal droppings of all fish species; however, the ability to survive gut passage and reattach to a substrate differed between algal taxa. While survival and reattachment approached zero for Phaeophyta and Chlorophyta, 76.4 % of the fragments belonging to the group Rhodophyta (mostly species in the order Gelidiaceae) survived gut passage, and were able to grow and reattach to the substrate by forming new rhizoids. Our results thus show that Gelidid algal species are dispersed by swimming herbivores. While the relative contribution of this mechanism to overall algal dispersal and recruitment in a wider ecological context remains unknown, our findings illustrate a previously undescribed mechanism of algal dispersal on coral reefs which is analogous to the dispersal of terrestrial plants, plant fragments, and seeds via herbivore ingestion and defecation.

2012
Choi, H, Mascuch SJ, Villa FA, Byrum T, Teasdale ME, Smith JE, Preskitt LB, Rowley DC, Gerwick L, Gerwick WH.  2012.  Honaucins A-C, Potent Inhibitors of Inflammation and Bacterial Quorum Sensing: Synthetic Derivatives and Structure-Activity Relationships. Chemistry & Biology. 19:589-598.   10.1016/j.chembiol.2012.03.014   AbstractWebsite

Honaucins A-C were isolated from the cyanobacterium Leptolyngbya crossbyana which was found overgrowing corals on the Hawaiian coast. Honaucin A consists of (S)-3-hydroxy-gamma-butyrolactone and 4-chlorocrotonic acid, which are connected via an ester linkage. Honaucin A and its two natural analogs exhibit potent inhibition of both bioluminescence, a quorum-sensing-dependent phenotype, in Vibrio harveyi BB120 and lipopolysaccharide-stimulated nitric oxide production in the murine macrophage cell line RAW264.7. The decrease in nitric oxide production was accompanied by a decrease in the transcripts of several proinflammatory cytokines, most dramatically interleukin-1 beta. Synthesis of honaucin A, as well as a number of analogs, and subsequent evaluation in anti-inflammation and quorum-sensing inhibition bioassays revealed the essential structural features for activity in this chemical class and provided analogs with greater potency in both assays.