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2019
Kelly, LW, Nelson CE, Haas AF, Naliboff DS, Calhoun S, Carlson CA, Edwards RA, Fox MD, Hatay M, Johnson MD, Kelly ELA, Lim YW, Macherla S, Quinlan ZA, Silva GGZ, Vermeij MJA, Zgliczynski B, Sandin SA, Smith JE, Rohwer F.  2019.  Diel population and functional synchrony of microbial communities on coral reefs. Nature Communications. 10   10.1038/s41467-019-09419-z   AbstractWebsite

On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs.

McNamara, DE, Cortale N, Edwards C, Eynaud Y, Sandin SA.  2019.  Insights into coral reef benthic dynamics from nonlinear spatial forecasting. Journal of the Royal Society Interface. 16   10.1098/rsif.2019.0047   AbstractWebsite

Nonlinear time-series forecasting, or empirical dynamic modelling, has been used extensively in the past two decades as a tool for distinguishing between random temporal behaviour and nonlinear deterministic dynamics. Previous authors have extended nonlinear time-series forecasting to continuous spatial data. Here, we adjust spatial forecasting to handle discrete data and apply the technique to explore the ubiquity of nonlinear determinism in irregular spatial configurations of coral and algal taxa from Palmyra Atoll, a relatively pristine reef in the central Pacific Ocean. We find that the spatial distributions of coral and algal taxa show signs of nonlinear determinism in some locations and that these signals can change through time. We introduce the hypothesis that nonlinear spatial determinism may be a signal of systems in intermediate developmental (i.e. successional) stages, with spatial randomness characterizing early (i.e. recruitment dominated) and late-successional (i.e. 'climax' or attractor) phases. Common state-based metrics that sum community response to environmental forcing lack resolution to detect dynamics of (potential) recovery phases; incorporating signal of spatial patterning among sessile taxa holds unique promise to elucidate dynamical characters of complex ecological systems, thereby enhancing study and response efforts.

2018
Fox, MD, Williams GJ, Johnson MD, Radice VZ, Zgliczynski BJ, Kelly ELA, Rohwer FL, Sandin SA, Smith JE.  2018.  Gradients in primary production predict trophic strategies of mixotrophic corals across spatial scales. Current Biology. 28:3355-+.   10.1016/j.cub.2018.08.057   AbstractWebsite

Mixotrophy is among the most successful nutritional strategies in terrestrial and marine ecosystems. The ability of organisms to supplement primary nutritional modes along continua of autotrophy and heterotrophy fosters trophic flexibility that can sustain metabolic demands under variable or stressful conditions. Symbiotic, reef-building corals are among the most broadly distributed and ecologically important mixotrophs, yet we lack a basic understanding of how they modify their use of autotrophy and heterotrophy across gradients of food availability. Here, we evaluate how one coral species, Pocillopora meandrina, supplements autotrophic nutrition through heterotrophy within an archipelago and test whether this pattern holds across species globally. Using stable isotope analysis (delta C-13) and satellite-derived estimates of nearshore primary production (chlorophylla, as a proxy for food availability), we show that P. meandrina incorporates a greater proportion of carbon via heterotrophy when more food is available across five central Pacific islands. We then show that this pattern is consistent globally using data from 15 coral species across 16 locations spanning the Caribbean Sea and the Indian and Pacific Oceans. Globally, surface chlorophyll-a explains 77% of the variation in coral heterotrophic nutrition, 86% for one genus across 10 islands, and 94% when controlling for coral taxonomy within archipelagos. These results demonstrate, for the first time, that satellite-derived estimates of nearshore primary production provide a globally relevant proxy for resource availability that can explain variation in coral trophic ecology. Thus, our model provides a pivotal step toward resolving the biophysical couplings between mixotrophic organisms and spatial patterns of resource availability in the coastal oceans.

Wood, CL, Zgliczynski BJ, Haupt AJ, Guerra AS, Micheli F, Sandin SA.  2018.  Human impacts decouple a fundamental ecological relationship-The positive association between host diversity and parasite diversity. Global Change Biology. 24:3666-3679.   10.1111/gcb.14159   AbstractWebsite

Human impacts on ecosystems can decouple the fundamental ecological relationships that create patterns of diversity in free-living species. Despite the abundance, ubiquity, and ecological importance of parasites, it is unknown whether the same decoupling effects occur for parasitic species. We investigated the influence of fishing on the relationship between host diversity and parasite diversity for parasites of coral reef fishes on three fished and three unfished islands in the central equatorial Pacific. Fishing was associated with a shallowing of the positive host-diversity-parasite-diversity relationship. This occurred primarily through negative impacts of fishing on the presence of complex life-cycle parasites, which created a biologically impoverished parasite fauna of directly transmitted parasites resilient to changes in host biodiversity. Parasite diversity appears to be decoupled from host diversity by fishing impacts in this coral reef ecosystem, which suggests that such decoupling might also occur for parasites in other ecosystems affected by environmental change.

Maire, E, Villeger S, Graham NAJ, Hoey AS, Cinner J, Ferse SCA, Aliaume C, Booth DJ, Feary DA, Kulbicki M, Sandin SA, Vigliola L, Mouillot D.  2018.  Community-wide scan identifies fish species associated with coral reef services across the Indo-Pacific. Proceedings of the Royal Society B-Biological Sciences. 285   10.1098/rspb.2018.1167   AbstractWebsite

Determining whether many functionally complementary species or only a subset of key species are necessary to maintain ecosystem functioning and services is a critical question in community ecology and biodiversity conservation. Identifying such key species remains challenging, especially in the tropics where many species co-occur and can potentially support the same or different processes. Here, we developed a new community-wide scan CWS) approach, analogous to the genome-wide scan, to identify fish species that significantly contribute, beyond the socio-environmental and species richness effects, to the biomass and coral cover on Indo-Pacific reefs. We found that only a limited set of species (51 out of approx. 400, = approx. 13%), belonging to various functional groups and evolutionary lineages, are strongly and positively associated with fish biomass and live coral cover. Many of these species have not previously been identified as functionally important, and thus may be involved in unknown, yet important, biological mechanisms that help sustain healthy and productive coral reefs. CWS has the potential to reveal species that are key to ecosystem functioning and services and to guide management strategies as well as new experiments to decipher underlying causal ecological processes.

Nakajima, R, Haas AF, Silveira CB, Kelly ELA, Smith JE, Sandin S, Kelly LW, Rohwer F, Nakatomi N, Kurihara H.  2018.  Release of dissolved and particulate organic matter by the soft coral Lobophytum and subsequent microbial degradation. Journal of Experimental Marine Biology and Ecology. 504:53-60.   10.1016/j.jembe.2018.02.008   AbstractWebsite

Understanding the release and remineralization of organic matter by benthic macroorganisms provides insight into nutrient cycling and microbial metabolism in coral reef environments. The release rate of particulate (POC) and dissolved organic carbon (DOC) by the soft coral Lobophytum crassum was quantified and subsequent bacterial growth rates determined in response to this resource, and compared with results from those of the common hard coral Acropora intermedia. The results of this study show that the soft coral released more DOC than POC into the surrounding seawater, similar to what was measured for the hard coral species. However, the soft coral-derived organic matter fostered a lower microbial growth rate with a lower growth efficiency compared to DOC and POC of hard corals, likely due to the lower C:N ratio of the organic matter derived from soft corals. These results suggest that soft coral exudates are relatively refractory compared to the mucus of hard corals. Possible phase shifts from hard to soft corals on degraded reefs may represent very different changes in microbial community dynamics and metabolism as compared to the widely studied coral-algal phase shifts.

Panovska, S, Constable CG, Brown MC.  2018.  Global and regional assessments of paleosecular variation activity over the past 100 ka. Geochemistry Geophysics Geosystems. 19:1559-1580.   10.1029/2017gc007271   AbstractWebsite

We present a global compilation of paleomagnetic data spanning the past 100 ka. Sediment data comprise 61,687 declinations, 70,936 inclinations, and 69,596 relative paleointensities. Many sites are located in the northern Atlantic and western Pacific, with approximately twice as many data from the Northern Hemisphere as from the Southern Hemisphere. The 14,954 volcanic and archeomagnetic data are sparse, especially in the Southern Hemisphere. Directional and intensity information are aggregated under the paleosecular variation (PSV) index to assess occurrence of excursions over the past 100 ka. The Laschamp excursion (approximate to 41 ka) is clearly defined across globally distributed sediment records with an average duration of 1,300 years. Regional stacks obtained using bootstrap resampling show a more pronounced Laschamp excursion in the Northern Hemisphere than in the Southern, and in the Atlantic Hemisphere compared with the Pacific. No anomalous indices occurred around the Mono Lake excursion or other periods in the bootstrap curves. This may result from low sedimentation rates, discrepancies in age scales, large age errors, and/or the lack of global character of any transitional events. These data and associated new uncertainty estimates for the sediment records provide a good foundation for global, time-dependent, spherical harmonic field modeling for the past 100 ka.

Williams, GJ, Sandin SA, Zgliczynski BJ, Fox MD, Gove JM, Rogers JS, Furby KA, Hartmann AC, Caldwell ZR, Price NN, Smith JE.  2018.  Biophysical drivers of coral trophic depth zonation. Marine Biology. 165   10.1007/s00227-018-3314-2   AbstractWebsite

Depth is used often as a proxy for gradients in energetic resources on coral reefs and for predicting patterns of community energy use. With increasing depth, loss of light can lead to a reduced reliance on autotrophy and an increased reliance on heterotrophy by mixotrophic corals. However, the generality of such trophic zonation varies across contexts. By combining high-resolution oceanographic measurements with isotopic analyses (delta C-13, delta N-15) of multiple producer and consumer levels across depths (10-30 m) at a central Pacific oceanic atoll, we show trophic zonation in mixotrophic corals can be both present and absent within the same reef system. Deep-water internal waves that deliver cool particulate-rich waters to shallow reefs occurred across all sites (2.5-5.6 events week(-1) at 30 m) but the majority of events remained depth-restricted (4.3-9.7% recorded at 30 m propagated to 10 m). In the absence of other particulate delivery, mixotrophs increased their relative degree of heterotrophy with increasing depth. However, where relatively long-lasting downwelling events (1.4-3.3 times the duration of any other site) occurred simultaneously, mixotrophs displayed elevated and consistent degrees of heterotrophy regardless of depth. Importantly, these long-lasting surface pulses were of a lagoonal origin, an area of rich heterotrophic resource supply. Under such circumstances, we hypothesize heterotrophic resource abundance loses its direct linkage with depth and, with resources readily available at all depths, trophic zonation is no longer present. Our results show that fine-scale intra-island hydrographic regimes and hydrodynamic connectivity between reef habitats contribute to explaining the context specific nature of coral trophic depth zonation in shallow reef ecosystems.

McCauley, DJ, Gellner G, Martinez ND, Williams RJ, Sandin SA, Micheli F, Mumby PJ, McCann KS.  2018.  On the prevalence and dynamics of inverted trophic pyramids and otherwise top-heavy communities. Ecology Letters. 21:439-454.   10.1111/ele.12900   AbstractWebsite

Classically, biomass partitioning across trophic levels was thought to add up to a pyramidal distribution. Numerous exceptions have, however, been noted including complete pyramidal inversions. Elevated levels of biomass top-heaviness (i.e. high consumer/resource biomass ratios) have been reported from Arctic tundra communities to Brazilian phytotelmata, and in species assemblages as diverse as those dominated by sharks and ants. We highlight two major pathways for creating top-heaviness, via: (1) endogenous channels that enhance energy transfer across trophic boundaries within a community and (2) exogenous pathways that transfer energy into communities from across spatial and temporal boundaries. Consumer-resource models and allometric trophic network models combined with niche models reveal the nature of core mechanisms for promoting top-heaviness. Outputs from these models suggest that top-heavy communities can be stable, but they also reveal sources of instability. Humans are both increasing and decreasing top-heaviness in nature with ecological consequences. Current and future research on the drivers of top-heaviness can help elucidate fundamental mechanisms that shape the architecture of ecological communities and govern energy flux within and between communities. Questions emerging from the study of top-heaviness also usefully draw attention to the incompleteness and inconsistency by which ecologists often establish definitional boundaries for communities.

Ruttenberg, B, Caselle JE, Estep AJ, Johnson AE, Marhaver KL, Richter LJ, Sandin SA, Vermeij MJA, Smith JE, Grenda D, Cannon A.  2018.  Ecological assessment of the marine ecosystems of Barbuda, West Indies: Using rapid scientific assessment to inform ocean zoning and fisheries management. Plos One. 13   10.1371/journal.pone.0189355   AbstractWebsite

To inform a community-based ocean zoning initiative, we conducted an intensive ecological assessment of the marine ecosystems of Barbuda, West Indies. We conducted 116 fish and 108 benthic surveys around the island, and measured the abundance and size structure of lobsters and conch at 52 and 35 sites, respectively. We found that both coral cover and fish biomass were similar to or lower than levels observed across the greater Caribbean; live coral cover and abundance of fishery target species, such as large snappers and groupers, was generally low. However, Barbuda lacks many of the high-relief forereef areas where similar work has been conducted in other Caribbean locations. The distribution of lobsters was patchy, making it difficult to quantify density at the island scale. However, the maximum size of lobsters was generally larger than in other locations in the Caribbean and similar to the maximum size reported 40 years ago. While the lobster population has clearly been heavily exploited, our data suggest that it is not as overexploited as in much of the rest of the Caribbean. Surveys of Barbuda's Codrington Lagoon revealed many juvenile lobsters, but none of legal size (95 mm carapace length), suggesting that the lagoon functions primarily as nursery habitat. Conch abundance and size on Barbuda were similar to that of other Caribbean islands. Our data suggest that many of the regional threats observed on other Caribbean islands are present on Barbuda, but some resources-particularly lobster and conch-may be less overexploited than on other Caribbean islands. Local management has the potential to provide sustainability for at least some of the island's marine resources. We show that a rapid, thorough ecological assessment can reveal clear conservation opportunities and facilitate rapid conservation action by providing the foundation for a community-driven policymaking process at the island scale.

2017
Knowles, B, Bailey B, Boling L, Breitbart M, Cobian-Guemes A, del Campo J, Edwards R, Felts B, Grasis J, Haas AF, Katira P, Kelly LW, Luque A, Nulton J, Paul L, Peters G, Robinett N, Sandin S, Segall A, Silveira C, Youle M, Rohwer F.  2017.  Variability and host density independence in inductions-based estimates of environmental lysogeny. Nature Microbiology. 2   10.1038/nmicrobiol.2017.64   AbstractWebsite

Temperate bacterial viruses (phages) may enter a symbiosis with their host cell, forming a unit called a lysogen. Infection and viral replication are disassociated in lysogens until an induction event such as DNA damage occurs, triggering viral-mediated lysis. The lysogen–lytic viral reproduction switch is central to viral ecology, with diverse ecosystem impacts. It has been argued that lysogeny is favoured in phages at low host densities. This paradigm is based on the fraction of chemically inducible cells (FCIC) lysogeny proxy determined using DNA-damaging mitomycin C inductions. Contrary to the established paradigm, a survey of 39 inductions publications found FCIC to be highly variable and pervasively insensitive to bacterial host density at global, within-environment and within-study levels. Attempts to determine the source(s) of variability highlighted the inherent complications in using the FCIC proxy in mixed communities, including dissociation between rates of lysogeny and FCIC values. Ultimately, FCIC studies do not provide robust measures of lysogeny or consistent evidence of either positive or negative host density dependence to the lytic–lysogenic switch. Other metrics are therefore needed to understand the drivers of the lytic–lysogenic decision in viral communities and to test models of the host density-dependent viral lytic–lysogenic switch.
Lysogenic dynamics can disassociate viral infection and production, leading to virus–host predator–prey feedbacks, densities and ecosystem impacts divergent from those predicted under lytic dynamics1,2,3. Although the majority of cultured laboratory and environmental bacterial strains are known lysogens4,5, quantifying the fraction of lysogens in natural mixed communities remains challenging. The prevalence of lysogeny is most commonly estimated by using the DNA-damaging agent mitomycin C to induce prophages (viruses that have established sustained intra- or extra-chromosomal residence in their hosts) to enter the lytic cycle and produce quantifiable viral progeny6,7. Lysogeny has been diagnosed using this technique in laboratory strains for half a century6,8. However, treatment of lysogens can yield induction, unsuccessful induction, or inhibition of host and viral production under different mitomycin C concentrations (Table 1)6 that vary on a strain-specific basis9. Inductions are difficult to interpret, even under single-strain laboratory conditions. Despite these challenges, in the 1990s Jiang and Paul4,10 extended this induction method from laboratory strains to bacterial isolates from mixed natural communities, showing that lysogeny is a common viral strategy in the environment (25–62.5% of strains were lysogens). Higher percentages were commonly observed under oligotrophic conditions than in eutrophic systems, suggesting links between the rate of lysogeny, nutrient regime and host density4,10.
Concurrent studies directly probed natural communities by adding mitomycin C into samples of sea water11,12. In those studies, the fraction of lysogenic cells (FLC, hereafter referred to as the fraction of chemically inducible cells, FCIC, due to disassociation of lysogeny and the induced fraction, as a percent of total cellular density) was estimated as
%FCIC=(Vi−Vc)/BC×100(1)(1)%FCIC=(Vi−Vc)/BC×100
using viral densities in the induced (Vi) and control (Vc) treatments, burst size B and host density C (cells per ml or g of sample) before incubation11,12,13. In contrast to earlier isolate-based studies, this mixed-community approach showed that either FCIC was insensitive to ecosystem nutrient status12 or was higher under eutrophic conditions11.
Subsequent research led to the consensus view that the frequency of lysogeny was inversely related to host density and nutrient availability14,15,16,17. This suggested that lysogeny provides a temporary refuge for viruses when hosts are starving and scarce14, seemingly providing a low-density lysogenic dynamic complementary to the modelled high-density lytic ‘kill-the-winner’ dynamic18. By contrast, recent work using extensive field direct counts, experiments and viromes (c.f. chemical induction) suggests that lysogeny is favoured when hosts are highly abundant and rapidly growing1. We call this model ‘piggyback-the-winner’. The association of high host densities with high rates of lysogeny reflects the benefits of lysogeny to hosts, including prophage-mediated immunity against further infection19,20, protection from protist predation via virulence factors, and gain of metabolic functions21,22,23.
Approximately 40 studies measuring rates of lysogeny in mixed natural communities using mitomycin C induction have been published in the twenty years since the pioneering work of Jiang and Paul4,10(Supplementary Table 1). We have compiled data from published environmental induction studies and found that FCIC is highly variable and seldom correlated with host density. Attempts to identify the source(s) of FCIC variability revealed issues with estimating the rates of lysogeny using mitomycin C induction. We propose that lysogeny and FCIC are not equivalent and that FCIC measurements obscure relationships between host density and lysogeny.

Edwards, CB, Eynaud Y, Williams GJ, Pedersen NE, Zgliczynski BJ, Gleason ACR, Smith JE, Sandin SA.  2017.  Large-area imaging reveals biologically driven non-random spatial patterns of corals at a remote reef. Coral Reefs. 36:1291-1305.   10.1007/s00338-017-1624-3   AbstractWebsite

For sessile organisms such as reef-building corals, differences in the degree of dispersion of individuals across a landscape may result from important differences in life-history strategies or may reflect patterns of habitat availability. Descriptions of spatial patterns can thus be useful not only for the identification of key biological and physical mechanisms structuring an ecosystem, but also by providing the data necessary to generate and test ecological theory. Here, we used an in situ imaging technique to create large-area photomosaics of 16 plots at Palmyra Atoll, central Pacific, each covering 100 m(2) of benthic habitat. We mapped the location of 44,008 coral colonies and identified each to the lowest taxonomic level possible. Using metrics of spatial dispersion, we tested for departures from spatial randomness. We also used targeted model fitting to explore candidate processes leading to differences in spatial patterns among taxa. Most taxa were clustered and the degree of clustering varied by taxon. A small number of taxa did not significantly depart from randomness and none revealed evidence of spatial uniformity. Importantly, taxa that readily fragment or tolerate stress through partial mortality were more clustered. With little exception, clustering patterns were consistent with models of fragmentation and dispersal limitation. In some taxa, dispersion was linearly related to abundance, suggesting density dependence of spatial patterning. The spatial patterns of stony corals are non-random and reflect fundamental life-history characteristics of the taxa, suggesting that the reef landscape may, in many cases, have important elements of spatial predictability.

Agius, MR, Rychert CA, Harmon N, Laske G.  2017.  Mapping the mantle transition zone beneath Hawaii from Ps receiver functions: Evidence for a hot plume and cold mantle downwellings. Earth and Planetary Science Letters. 474:226-236.   10.1016/j.epsl.2017.06.033   AbstractWebsite

Hawaii is the archetypal example of hotspot volcanism. Classic plume theory suggests a vertical plume ascent from the core-mantle boundary to the surface. However, recently it has been suggested that the plume path may be more complex. Determining the exact trajectory of the Hawaiian plume seismic anomaly in the mantle has proven challenging. We determine P-to-S (Ps) receiver functions to illuminate the 410- and 660-km depth mantle discontinuities beneath the Hawaiian Islands using waveforms recorded on land and ocean-bottom seismometers, applying new corrections for tilt and coherence to the ocean bottom data. Our 3-D depth-migrated maps provide enhanced lateral resolution of the mantle transition zone discontinuities. The 410 discontinuity is characterised by a deepened area beneath central Hawaii, surrounded by an elevated shoulder. At the 660 discontinuity, shallow topography is located to the north and far south of the islands, and a deep topographic anomaly is located far west and east. The transition zone thickness varies laterally by 13 km depth: thin beneath north-central Hawaii and thick farther away in a horseshoe-like feature. We infer that at 660-km depth a broad or possibly a double region of upwelling converges into a single plume beneath central Hawaii at 410-km depth. As the plume rises farther, uppermost mantle melting and flow results in the downwelling of cold material, down to at least 410 km surrounding the plume stem. This result in the context of others supports complex plume dynamics including a possible non-vertical plume path and adjacent mantle downwellings. (C) 2017 The Author(s). Published by Elsevier B.V.

Kelly, ELA, Eynaud Y, Williams ID, Sparks RT, Dailer ML, Sandin SA, Smith JE.  2017.  A budget of algal production and consumption by herbivorous fish in an herbivore fisheries management area, Maui, Hawaii. Ecosphere. 8   10.1002/ecs2.1899   AbstractWebsite

The relative rates of carbon fixed by primary producers vs. consumption by primary consumers shape the community of organisms in ecosystems. On coral reefs, it is important to understand the demography of algae, given known competitive dynamics with reef-building corals. Numerous studies have shown that fleshy algal abundance is enhanced in the absence of top-down control by herbivores on coral reefs. However, fewer studies have quantified and compared rates of production by the benthic fleshy algal community and consumption by herbivores. Here, we estimate a budget for fleshy algal growth and herbivorous fish consumption on a Hawaiian coral reef based upon integration of field-measured and taxonomically specific variables. Data were collected at Kahekili Herbivore Fisheries Management Area, Maui, established in 2009, in which taking of herbivorous fish and urchins is prohibited. Daily algal production was determined by quantifying benthic community composition, standing stock of algal biomass, and growth rates of common algal components. Consumption was determined using distributions of biomass and size classes of herbivorous fish species, consumption rates of herbivores on different algal species, and herbivore bite sizes. Our results show that throughout the first five years of herbivore protection, algal production consistently exceeded the grazing capacity of the herbivorous fish assemblage, but by a diminishing margin since 2010 (consumption 20.8% of production) to the end of the study in 2014 (consumption 67.0% of production). Further, larger size classes of herbivorous fishes in the scraper/excavator herbivore guild contributed more to consumption in later years, which could have additional feedbacks that promote reef-building taxa. Projecting the budget using data from a neighboring decades-long protected herbivorous fish assemblage indicated that the production and consumption budget for Kahekili could become balanced in future with continued management.

Nicklisch, SCT, Bonito LT, Sandin S, Hamdoun A.  2017.  Geographic differences in persistent organic pollutant levels of yellowfin tuna. Environ Health Perspect. 125:067014.   10.1289/ehp518   Abstract

BACKGROUND: Fish are a source of persistent organic pollutants (POPs) in the human diet. Although species, trophic level, and means of production are typically considered in predicting fish pollutant load, and thus recommendations of consumption, capture location is usually not accounted for. OBJECTIVES: Yellowfin tuna (Thunnus albacares) are harvested from across the world's oceans and are widely consumed. Here, we determined geographic variation in the overall mass, concentration, and composition of POPs in yellowfin and examined the differences in levels of several POP congeners of potential relevance to human health. METHODS: We sampled dorsal muscle of 117 yellowfin tuna from 12 locations worldwide, and measured POP levels using combined liquid or gas chromatography and mass spectrometry according to U.S. Environmental Protection Agency standard procedures. RESULTS: POP levels varied significantly among sites, more than 36-fold on a mass basis. Individual fish levels ranged from 0.16 to wet weight and lipid-normalized concentrations from . Levels of 10 congeners that interfere with the cellular defense protein P-glycoprotein, termed transporter interfering compounds (TICs), ranged from 0.05 to wet weight and from in tuna lipid. Levels of TICs, and their individual congeners, were strongly associated with the overall POP load. Risk-based analysis of several carcinogenic POPs indicated that the fish with the highest levels of these potentially harmful compounds were clustered at specific geographic locations. CONCLUSIONS: Capture location is an important consideration when assessing the level and risk of human exposure to POPs through ingestion of wild fish.

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.

Zgliczynski, BJ, Sandin SA.  2017.  Size-structural shifts reveal intensity of exploitation in coral reef fisheries. Ecological Indicators. 73:411-421.   10.1016/j.ecolind.2016.09.045   AbstractWebsite

Fisheries exploitation represents a considerable threat to coral reef fish resources because even modest levels of extraction can alter ecological dynamics via shifts of stock size, species composition, and size-structure of the fish assemblage. Although species occupying higher trophic groups are known to suffer the majority of exploitative effects, changes in composition among lower trophic groups may be major, though are not frequently explored. Using size-based biomass spectrum analysis, we investigate the effects of fishing on the size-structure of coral reef fish assemblages spanning four geopolitical regions and determine if patterns of exploitation vary across trophic groups. Our analyses reveal striking evidence for the variety of effects fisheries exploitation can have on coral reef fish assemblages. When examining biomass spectra across the entire fish assemblage we found consistent evidence of size-specific exploitation, in which large-bodied individuals experience disproportionate reductions. The pattern was paralleled by and likely driven by, strongly size-specific reductions among top predators. In contrast, evidence of exploitation patterns was variable among lower trophic groups, in many cases including evidence of reductions across all size classes. The breadth of size classes and trophic groups that showed evidence of exploitation related positively to local human population density and diversity of fishing methods employed. Our findings highlight the complexity of coral reef fisheries and that the effects of exploitation on coral reefs can be realized throughout the entire fish assemblage, across multiple trophic groups and not solely restricted to large-bodied top-predators. Size-specific changes among fishes of lower trophic groups likely lead to altered ecological functioning of heavily exploited coral reefs. Together these findings reinforce the value of taking a multi-trophic group approach to monitoring and managing coral reef fisheries. (C) 2016 Elsevier Ltd. All rights reserved.

2016
Cinner, JE, Huchery C, MacNeil AM, Graham NAJ, McClanahan TR, Maina J, Maire E, Kittinger JN, Hicks CC, Mora C, Allison EH, D’Agata S, Hoey A, Feary DA, Crowder L, Williams ID, Kulbicki M, Vigliola L, Wantiez L, Edgar G, Stuart-Smith RD, Sandin SA, Green AL, Hardt MJ, Beger M, Friedlander A, Campbell SJ, Holmes KE, Wilson SK, Brokovich E, Brooks AJ, Cruz-Motta JJ, Booth DJ, Chabanet P, Gough C, Tupper M, Ferse SCA, Sumaila RU, Mouillot D.  2016.  Bright spots among the world’s coral reefs. Nature. 535:416-419.: Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.   10.1038/nature18607   AbstractWebsite

Ongoing declines in the structure and function of the world’s coral reefs1, 2 require novel approaches to sustain these ecosystems and the millions of people who depend on them3. A presently unexplored approach that draws on theory and practice in human health and rural development4, 5 is to systematically identify and learn from the ‘outliers’—places where ecosystems are substantially better (‘bright spots’) or worse (‘dark spots’) than expected, given the environmental conditions and socioeconomic drivers they are exposed to. Here we compile data from more than 2,500 reefs worldwide and develop a Bayesian hierarchical model to generate expectations of how standing stocks of reef fish biomass are related to 18 socioeconomic drivers and environmental conditions. We identify 15 bright spots and 35 dark spots among our global survey of coral reefs, defined as sites that have biomass levels more than two standard deviations from expectations. Importantly, bright spots are not simply comprised of remote areas with low fishing pressure; they include localities where human populations and use of ecosystem resources is high, potentially providing insights into how communities have successfully confronted strong drivers of change. Conversely, dark spots are not necessarily the sites with the lowest absolute biomass and even include some remote, uninhabited locations often considered near pristine6. We surveyed local experts about social, institutional, and environmental conditions at these sites to reveal that bright spots are characterized by strong sociocultural institutions such as customary taboos and marine tenure, high levels of local engagement in management, high dependence on marine resources, and beneficial environmental conditions such as deep-water refuges. Alternatively, dark spots are characterized by intensive capture and storage technology and a recent history of environmental shocks. Our results suggest that investments in strengthening fisheries governance, particularly aspects such as participation and property rights, could facilitate innovative conservation actions that help communities defy expectations of global reef degradation.

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.

Eynaud, Y, McNamara DE, Sandin SA.  2016.  Herbivore space use influences coral reef recovery. Royal Society Open Science. 3   10.1098/rsos.160262   AbstractWebsite

Herbivores play an important role in marine communities. On coral reefs, the diversity and unique feeding behaviours found within this functional group can have a comparably diverse set of impacts in structuring the benthic community. Here, using a spatially explicit model of herbivore foraging, we explore how the spatial pattern of grazing behaviours impacts the recovery of a reef ecosystem, considering movements at two temporal scales-short term (e.g. daily foraging patterns) and longer term (e.g. monthly movements across the landscape). Model simulations suggest that more spatially constrained herbivores are more effective at conferring recovery capability by providing a favourable environment to coral recruitment and growth. Results also show that the composition of food available to the herbivore community is linked directly to the pattern of space use by herbivores. To date, most studies of variability among the impacts of herbivore species have considered the diversity of feeding modes and mouthparts. Our work provides a complementary view of spatial patterns of foraging, revealing that variation in movement behaviours alone can affect patterns of benthic change, and thus broadens our view of realized links between herbivore diversity and reef recovery.

Nicklisch, SCT, Rees SD, McGrath AP, Gökirmak T, Bonito LT, Vermeer LM, Cregger C, Loewen G, Sandin S, Chang G, Hamdoun A.  2016.  Global marine pollutants inhibit P-glycoprotein: Environmental levels, inhibitory effects, and cocrystal structure. Science Advances. 2   10.1126/sciadv.1600001   Abstract

The world’s oceans are a global reservoir of persistent organic pollutants to which humans and other animals are exposed. Although it is well known that these pollutants are potentially hazardous to human and environmental health, their impacts remain incompletely understood. We examined how persistent organic pollutants interact with the drug efflux transporter P-glycoprotein (P-gp), an evolutionarily conserved defense protein that is essential for protection against environmental toxicants. We identified specific congeners of organochlorine pesticides, polychlorinated biphenyls, and polybrominated diphenyl ethers that inhibit mouse and human P-gp, and determined their environmental levels in yellowfin tuna from the Gulf of Mexico. In addition, we solved the cocrystal structure of P-gp bound to one of these inhibitory pollutants, PBDE (polybrominated diphenyl ether)–100, providing the first view of pollutant binding to a drug transporter. The results demonstrate the potential for specific binding and inhibition of mammalian P-gp by ubiquitous congeners of persistent organic pollutants present in fish and other foods, and argue for further consideration of transporter inhibition in the assessment of the risk of exposure to these chemicals.

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.

Caldwell, ZR, Zgliczynski BJ, Williams GJ, Sandin SA.  2016.  Reef fish survey techniques: Assessing the potential for standardizing methodologies. Plos One. 11   10.1371/journal.pone.0153066   AbstractWebsite

Dramatic changes in populations of fishes living on coral reefs have been documented globally and, in response, the research community has initiated efforts to assess and monitor reef fish assemblages. A variety of visual census techniques are employed, however results are often incomparable due to differential methodological performance. Although comparability of data may promote improved assessment of fish populations, and thus management of often critically important nearshore fisheries, to date no standardized and agreed-upon survey method has emerged. This study describes the use of methods across the research community and identifies potential drivers of method selection. An online survey was distributed to researchers from academic, governmental, and non-governmental organizations internationally. Although many methods were identified, 89% of survey-based projects employed one of three methods-belt transect, stationary point count, and some variation of the timed swim method. The selection of survey method was independent of the research design (i.e., assessment goal) and region of study, but was related to the researcher's home institution. While some researchers expressed willingness to modify their current survey protocols to more standardized protocols (76%), their willingness decreased when methodologies were tied to long-term datasets spanning five or more years. Willingness to modify current methodologies was also less common among academic researchers than resource managers. By understanding both the current application of methods and the reported motivations for method selection, we hope to focus discussions towards increasing the comparability of quantitative reef fish survey data.

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'.

Bonito, LT, Hamdoun A, Sandin SA.  2016.  Evaluation of the global impacts of mitigation on persistent, bioaccumulative and toxic pollutants in marine fish. Peerj. 4   10.7717/peerj.1573   AbstractWebsite

Although persistent, bioaccumulative and toxic pollutants (PBTs) are well-studied individually their distribution and variability on a global scale are largely unknown particularly in marine fish. Using 2,662 measurements collected from peer-reviewed literature spanning 1969-2012, we examined variability of five classes of PBTs, considering effects of geography, habitat, and trophic level on observed concentrations. While we see large-scale spatial patterning in some PBTs (chlordanes, polychlorinated biphenyls), habitat type and trophic level did not contribute to significant patterning, with the exception of mercury. We further examined patterns of change in PBT concentration as a function of sampling year. All PBTs showed significant declines in concentration levels through time, ranging from 15-30% reduction per decade across PBT groups. Despite consistent evidence of reductions, variation in pollutant concentration remains high, indicating ongoing consumer risk of exposure to fish with pollutant levels exceeding EPA screening values. The temporal trends indicate that mitigation programs are leffective, but that global levels decline slowly. In order for monitoring efforts to provide more targeted assessments of risk to PBT exposure, these data highlight an urgent need for improved replication and standardization of pollutant monitoring protocols for marine finfish.