Fox Michael D.

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Fox

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Michael D.

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0000-0002-5004-1025

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Now showing 1 - 12 of 12

Coral reef biofilm bacterial diversity and successional trajectories are structured by reef benthic organisms and shift under chronic nutrient enrichment

(Nature Research, 2021-12-01) Remple, Kristina L. ; Silbiger, Nyssa J. ; Quinlan, Zachary A. ; Fox, Michael D. ; Wegley Kelly, Linda ; Donahue, Megan J. ; Nelson, Craig E.

Work on marine biofilms has primarily focused on host-associated habitats for their roles in larval recruitment and disease dynamics; little is known about the factors regulating the composition of reef environmental biofilms. To contrast the roles of succession, benthic communities and nutrients in structuring marine biofilms, we surveyed bacteria communities in biofilms through a six-week succession in aquaria containing macroalgae, coral, or reef sand factorially crossed with three levels of continuous nutrient enrichment. Our findings demonstrate how biofilm successional trajectories diverge from temporal dynamics of the bacterioplankton and how biofilms are structured by the surrounding benthic organisms and nutrient enrichment. We identify a suite of biofilm-associated bacteria linked with the orthogonal influences of corals, algae and nutrients and distinct from the overlying water. Our results provide a comprehensive characterization of marine biofilm successional dynamics and contextualize the impact of widespread changes in reef community composition and nutrient pollution on biofilm community structure.
Characterizing energy flow in kelp forest food webs: a geochemical review and call for additional research

(Wiley Open Access, 2021-09-01) Elliott Smith, Emma A. ; Fox, Michael D.

Kelp forests are highly productive coastal habitats that serve as biodiversity hotspots and provide valuable ecosystem services. Despite being one the largest marine biomes, kelp forests have been drastically understudied relative to other marine systems. Notably, while the role of kelp as habitat-forming, or ‘foundation species', is well-documented, a comprehensive understanding of kelp forest food web structure is lacking, particularly regarding the importance of kelp-derived energy/nutrients to consumers. Here, we provide a biogeographic perspective on the energetic underpinning of kelp forests based on published literature. We targeted studies which used geochemical proxies – stable isotope analysis – to examine the transfer of carbon from kelp to local consumers. These studies (n = 94) were geographically skewed, with > 40% from Northern European Seas and Temperate Northeast Pacific. Quantitative estimates for the percentage of kelp energy (or kelp + macroalgae if sources were pooled) incorporated by local consumers came from 43 publications, which studied 141 species and 35 broader taxonomic groups. We examined these data for trends among functional groups and across upwelling regimes. No patterns are evident at present, perhaps due to the paucity or variability of available data. However, energetic subsides from kelps clearly support a wide range of diverse taxa around the globe. We also characterized biogeographic patterns in δ13C values of kelps and particulate organic matter (POM, a phytoplankton proxy), to evaluate potential limitations of stable isotope analysis in disentangling the relative contributions of pelagic versus benthic resources to coastal food webs. Globally, kelps and POM differed by > 4.5‰, but there was substantial variation among regions and kelp species. Accordingly, we discuss advances in stable isotope techniques which are facilitating more precise analysis of these complex energetic pathways. We end by proposing four main avenues of critical future research that will shed light on the resilience of these communities to global change.
Increasing coral reef resilience through successive marine heatwaves

(American Geophysical Union, 2021-08-30) Fox, Michael D. ; Cohen, Anne L. ; Rotjan, Randi ; Mangubhai, Sangeeta ; Sandin, Stuart A. ; Smith, Jennifer E. ; Thorrold, Simon R. ; Dissly, Laura ; Mollica, Nathaniel R. ; Obura, David

Ocean warming is causing declines of coral reefs globally, raising critical questions about the potential for corals to adapt. In the central equatorial Pacific, reefs persisting through recurrent El Niño heatwaves hold important clues. Using an 18-year record of coral cover spanning three major bleaching events, we show that the impact of thermal stress on coral mortality within the Phoenix Islands Protected Area (PIPA) has lessened over time. Disproportionate survival of extreme thermal stress during the 2009–2010 and 2015–2016 heatwaves, relative to that in 2002–2003, suggests that selective mortality through successive heatwaves may help shape coral community responses to future warming. Identifying and facilitating the conditions under which coral survival and recovery can keep pace with rates of warming are essential first steps toward successful stewardship of coral reefs under 21st century climate change.
Benthic assemblages are more predictable than fish assemblages at an island scale

(Springer, 2022-05-30) Sandin, Stuart A. ; Alcantar, Esmeralda ; Clark, Randy ; de León, Ramón ; Dilrosun, Faisal ; Edwards, Clinton B. ; Estep, Andrew J. ; Eynaud, Yoan ; French, Beverly J. ; Fox, Michael D. ; Grenda, Dave ; Hamilton, Scott L. ; Kramp, Heather ; Marhaver, Kristen L. ; Miller, Scott D. ; Roach, Ty N. F. ; Seferina, Gisette ; Silveira, Cynthia B. ; Smith, Jennifer E. ; Zgliczynski, Brian J. ; Vermeij, Mark J. A.

Decades of research have revealed relationships between the abundance of coral reef taxa and local conditions, especially at small scales. However, a rigorous test of covariation requires a robust dataset collected across wide environmental or experimental gradients. Here, we surveyed spatial variability in the densities of major coral reef functional groups at 122 sites along a 70 km expanse of the leeward, forereef habitat of Curaçao in the southern Caribbean. These data were used to test the degree to which spatial variability in community composition could be predicted based on assumed functional relationships and site-specific anthropogenic, physical, and ecological conditions. In general, models revealed less power to describe the spatial variability of fish biomass than cover of reef builders (R2 of best-fit models: 0.25 [fish] and 0.64 [reef builders]). The variability in total benthic cover of reef builders was best described by physical (wave exposure and reef relief) and ecological (turf algal height and coral recruit density) predictors. No metric of anthropogenic pressure was related to spatial variation in reef builder cover. In contrast, total fish biomass showed a consistent (albeit weak) association with anthropogenic predictors (fishing and diving pressure). As is typical of most environmental gradients, the spatial patterns of both fish biomass density and reef builder cover were spatially autocorrelated. Residuals from the best-fit model for fish biomass retained a signature of spatial autocorrelation while the best-fit model for reef builder cover removed spatial autocorrelation, thus reinforcing our finding that environmental predictors were better able to describe the spatial variability of reef builders than that of fish biomass. As we seek to understand spatial variability of coral reef communities at the scale of most management units (i.e., at kilometer- to island-scales), distinct and scale-dependent perspectives will be needed when considering different functional groups.
Offshore pelagic subsidies dominate carbon inputs to coral reef predators

(American Association for the Advancement of Science, 2021-02-19) Skinner, Christina ; Mill, Aileen C. ; Fox, Michael D. ; Newman, Steve P. ; Zhu, Yongguan ; Kuhl, Alison ; Polunin, Nicholas V. C.

Coral reefs were traditionally perceived as productive hot spots in oligotrophic waters. While modern evidence indicates that many coral reef food webs are heavily subsidized by planktonic production, the pathways through which this occurs remain unresolved. We used the analytical power of carbon isotope analysis of essential amino acids to distinguish between alternative carbon pathways supporting four key reef predators across an oceanic atoll. This technique separates benthic versus planktonic inputs, further identifying two distinct planktonic pathways (nearshore reef-associated plankton and offshore pelagic plankton), and revealing that these reef predators are overwhelmingly sustained by offshore pelagic sources rather than by reef sources (including reef-associated plankton). Notably, pelagic reliance did not vary between species or reef habitats, emphasizing that allochthonous energetic subsidies may have system-wide importance. These results help explain how coral reefs maintain exceptional productivity in apparently nutrient-poor tropical settings, but also emphasize their susceptibility to future ocean productivity fluctuations.
Linking variation in planktonic primary production to coral reef fish growth and condition

(The Royal Society, 2022-08-31) Roche, Ronan C. ; Heenan, Adel ; Taylor, Brett M. ; Schwarz, Jill N. ; Fox, Michael D. ; Southworth, Lucy K. ; Williams, Gareth J. ; Turner, John R.

Within low-nutrient tropical oceans, islands and atolls with higher primary production support higher fish biomass and reef organism abundance. External energy subsidies can be delivered onto reefs via a range of physical mechanisms. However, the influence of spatial variation in primary production on reef fish growth and condition is largely unknown. It is not yet clear how energy subsidies interact with reef depth and slope. Here we test the hypothesis that with increased proximity to deep-water oceanic nutrient sources, or at sites with shallower reef slopes, parameters of fish growth and condition will be higher. Contrary to expectations, we found no association between fish growth rate and sites with higher mean chlorophyll-a values. There were no differences in fish δ15N or δ13C values between depths. The relationship between fish condition and primary production was influenced by depth, driven by increased fish condition at shallow depths within a primary production ‘hotspot’ site. Carbon δ13C was depleted with increasing primary production, and interacted with reef slope. Our results indicate that variable primary production did not influence growth rates in planktivorous Chromis fieldi within 10–17.5 m depth, but show site-specific variation in reef physical characteristics influencing fish carbon isotopic composition.
Brilliantia kiribatiensis, a new genus and species of Cladophorales (Chlorophyta) from the remote coral reefs of the Southern Line Islands, Pacific Ocean

(Wiley, 2021-12-12) Leliaert, Frederik ; Kelly, Emily L. A. ; Janouškovec, Jan ; Fox, Michael D. ; Johnson, Maggie D. ; Redfern, Farran M. ; Eria, Taati ; Haas, Andreas F. ; Sala, Enric ; Sandin, Stuart A. ; Smith, Jennifer E.

The marine green alga Brilliantia kiribatiensis gen. et sp. nov. is described from samples collected from the coral reefs of the Southern Line Islands, Republic of Kiribati, Pacific Ocean. Phylogenetic analysis of sequences of the large- and small-subunit rDNA and the rDNA internal transcribed spacer region revealed that Brilliantia is a member of the Boodleaceae (Cladophorales), containing the genera Apjohnia, Boodlea, Cladophoropsis, Chamaedoris, Phyllodictyon, and Struvea. Within this clade it formed a distinct lineage, sister to Struvea elegans, but more distantly related to the bona fide Struvea species (including the type S. plumosa). Brilliantia differs from the other genera by having a very simple architecture forming upright, unbranched, single-celled filaments attached to the substratum by a rhizoidal mat. Cell division occurs by segregative cell division only at the onset of reproduction. Based on current sample collection, B. kiribatiensis seems to be largely restricted to the Southern Line Islands, although it was also observed on neighboring islands, including Orona Atoll in the Phoenix Islands of Kiribati, and the Rangiroa and Takapoto Atolls in the Tuamotus of French Polynesia. This discovery highlights the likeliness that there is still much biodiversity yet to be discovered from these remote and pristine reefs of the central Pacific.
Evaluating coral trophic strategies using fatty acid composition and indices

(Public Library of Science, 2019-09-11) Radice, Veronica Z. ; Brett, Michael T. ; Fry, Brian ; Fox, Michael D. ; Hoegh-Guldberg, Ove ; Dove, Sophie G.

The ecological success of shallow water reef-building corals has been linked to the symbiosis between the coral host and its dinoflagellate symbionts (herein ‘symbionts’). As mixotrophs, symbiotic corals depend on nutrients 1) transferred from their photosynthetic symbionts (autotrophy) and 2) acquired by host feeding on particulate organic resources (heterotrophy). However, coral species differ in the extent to which they depend on heterotrophy for nutrition and these differences are typically poorly defined. Here, a multi-tracer fatty acid approach was used to evaluate the trophic strategies of three species of common reef-building coral (Galaxea fascicularis, Pachyseris speciosa, and Pocillopora verrucosa) whose trophic strategies had previously been identified using carbon stable isotopes. The composition and various indices of fatty acids were compared to examine the relative contribution of symbiont autotrophy and host heterotrophy in coral energy acquisition. A linear discriminant analysis (LDA) was used to estimate the contribution of polyunsaturated fatty acids (PUFA) derived from various potential sources to the coral hosts. The total fatty acid composition and fatty acid indices revealed differences between the more heterotrophic (P. verrucosa) and more autotrophic (P. speciosa) coral hosts, with the coral host G. fascicularis showing overlap with the other two species and greater variability overall. For the more heterotrophic P. verrucosa, the fatty acid indices and LDA results both indicated a greater proportion of copepod-derived fatty acids compared to the other coral species. Overall, the LDA estimated that PUFA derived from particulate resources (e.g., copepods and diatoms) comprised a greater proportion of coral host PUFA in contrast to the lower proportion of symbiont-derived PUFA. These estimates provide insight into the importance of heterotrophy in coral nutrition, especially in productive reef systems. The study supports carbon stable isotope results and demonstrates the utility of fatty acid analyses for exploring the trophic strategies of reef-building corals.
Percent cover of benthic functional groups in the Phoenix Islands Protected Area (PIPA) from 2009, 2012, 2015, and 2018

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2022-11-29) Fox, Michael D. ; Cohen, Anne L.

This dataset includes percent cover of benthic functional groups in the Phoenix Islands Protected Area (PIPA). Percent cover of reef-building coral was quantified using photoquadrat transects conducted during 2009, 2012, 2015, and 2018 following standard Pacific coral reef monitoring protocols. Areas of study include: Phoenix Islands, Kiribati. Kanton Island (2.8 S, 171.6 W), Rawaki Island (3.7 S 170.7 W), Nikumaroro Island (4.7 S, 174.5 W), Orona Island (4.5 S, 172.2 W). These data were published in Fox et al., 2021 (DOI: 10.1029/2021GRL094128). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/863410
Ecophysiology of coral reef primary producers across an upwelling gradient in the tropical central Pacific

(Public Library of Science, 2020-02-04) Johnson, Maggie D. ; Fox, Michael D. ; Kelly, Emily L. A. ; Zgliczynski, Brian J. ; Sandin, Stuart A. ; Smith, Jennifer E.

Upwelling is an important source of inorganic nutrients in marine systems, yet little is known about how gradients in upwelling affect primary producers on coral reefs. The Southern Line Islands span a natural gradient of inorganic nutrient concentrations across the equatorial upwelling region in the central Pacific. We used this gradient to test the hypothesis that benthic autotroph ecophysiology is enhanced on nutrient-enriched reefs. We measured metabolism and photophysiology of common benthic taxa, including the algae Porolithon, Avrainvillea, and Halimeda, and the corals Pocillopora and Montipora. We found that temperature (27.2–28.7°C) was inversely related to dissolved inorganic nitrogen (0.46–4.63 μM) and surface chlorophyll a concentrations (0.108–0.147 mg m-3), which increased near the equator. Contrary to our prediction, ecophysiology did not consistently track these patterns in all taxa. Though metabolic rates were generally variable, Porolithon and Avrainvillea photosynthesis was highest at the most productive and equatorial island (northernmost). Porolithon photosynthetic rates also generally increased with proximity to the equator. Photophysiology (maximum quantum yield) increased near the equator and was highest at northern islands in all taxa. Photosynthetic pigments also were variable, but chlorophyll a and carotenoids in Avrainvillea and Montipora were highest at the northern islands. Phycobilin pigments of Porolithon responded most consistently across the upwelling gradient, with higher phycoerythrin concentrations closer to the equator. Our findings demonstrate that the effects of in situ nutrient enrichment on benthic autotrophs may be more complex than laboratory experiments indicate. While upwelling is an important feature in some reef ecosystems, ancillary factors may regulate the associated consequences of nutrient enrichment on benthic reef organisms.
Hourly temperature data from deployments between 2012 and 2018 from three of the Phoenix Islands

(Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2022-11-29) Fox, Michael D. ; Cohen, Anne L.

This dataset includes hourly temperature data from deployments of HOBO pendant temperature loggers at three of the Phoenix Islands (Kiribati: Kanton Island, Rawaki Island, and Nikumaroro Island) between 2012 and 2018. These data were published in Fox et al., 2021 (DOI: 10.1029/2021GRL094128). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/863421
Palau's warmest reefs harbor thermally tolerant corals that thrive across different habitats

(Nature Research, 2022-12-21) Rivera, Hanny E. ; Cohen, Anne L. ; Thompson, Janelle R. ; Baums, Iliana B. ; Fox, Michael D. ; Meyer-Kaiser, Kirstin S.

Ocean warming is killing corals, but heat-tolerant populations exist; if protected, they could replenish affected reefs naturally or through restoration. Palau's Rock Islands experience consistently higher temperatures and extreme heatwaves, yet their diverse coral communities bleach less than those on Palau's cooler outer reefs. Here, we combined genetic analyses, bleaching histories and growth rates of Porites cf. lobata colonies to identify thermally tolerant genotypes, map their distribution, and investigate potential growth trade-offs. We identified four genetic lineages of P. cf. lobata. On Palau's outer reefs, a thermally sensitive lineage dominates. The Rock Islands harbor two lineages with enhanced thermal tolerance; one of which shows no consistent growth trade-off and also occurs on several outer reefs. This suggests that the Rock Islands provide naturally tolerant larvae to neighboring areas. Finding and protecting such sources of thermally-tolerant corals is key to reef survival under 21century climate change.

Fox Michael D.

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