Biological Oxygen Demand Optode Analysis of Coral Reef-Associated Microbial Communities Exposed to Algal Exudates

Algae-derived dissolved organic matter has been hypothesized to induce mortality of reef building corals. One proposed killing mechanism is a zone of hypoxia created by rapidly growing microbes. To investigate this hypothesis, biological oxygen demand (BOD) optodes were used to quantify the change in oxygen concentrations of microbial communities following exposure to exudates generated by turf algae and crustose coralline algae (CCA). BOD optodes were embedded with microbial communities cultured from Montastraea annularis and Mussismilia hispida, and respiration was measured during exposure to turf and CCA exudates. The oxygen concentrations along the optodes were visualized with a low-cost Submersible Oxygen Optode Recorder (SOOpR) system. With this system we observed that exposure to exudates derived from turf algae stimulated higher oxygen drawdown by the coral-associated bacteria than CCA exudates or seawater controls. Furthermore, in both turf and CCA exudate treatments, all microbial communities (coral-, algae-associated and pelagic) contributed significantly to the observed oxygen drawdown. This suggests that the driving factor for elevated oxygen consumption rates is the source of exudates rather than the initially introduced microbial community. Our results demonstrate that exudates from turf algae may contribute to hypoxia-induced coral stress in two different coral genera as a result of increased biological oxygen demand of the local microbial community. Additionally, the SOOpR system developed here can be applied to measure the BOD of any culturable microbe or microbial community

Benthic assemblages are more predictable than fish assemblages at an island scale

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sandin, S. A., Alcantar, E., Clark, R., de Leon, R., Dilrosun, F., Edwards, C. B., Estep, A. J., Eynaud, Y., French, B. J., Fox, M. D., Grenda, D., Hamilton, S. L., Kramp, H., Marhaver, K. L., Miller, S. D., Roach, T. N. F., Seferina, G., Silveira, C. B., Smith, J. E., Zgliczynski, B. J., & Vermeij, M. J. A. Benthic assemblages are more predictable than fish assemblages at an island scale. Coral Reefs, 41, (2022.): 1031–1043, https://doi.org/10.1007/s00338-022-02272-5.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.This research and the larger efforts of Blue Halo Curacao were supported by funding from the Waitt Institute and with permissions from the Government of Curacao, Ministry of Health, Environment, and Nature. Field logistics were further supported by the Waitt Institute vessel crew, CARMABI Foundation, The Dive Shop Curacao, and Dive Charter Curacao

Coral larvae move toward reef sounds

Free-swimming larvae of tropical corals go through a critical life-phase when they return from the open ocean to select a suitable settlement substrate. During the planktonic phase of their life cycle, the behaviours of small coral larvae (<1 mm) that influence settlement success are difficult to observe in situ and are therefore largely unknown. Here, we show that coral larvae respond to acoustic cues that may facilitate detection of habitat from large distances and from upcurrent of preferred settlement locations. Using in situ choice chambers, we found that settling coral larvae were attracted to reef sounds, produced mainly by fish and crustaceans, which we broadcast underwater using loudspeakers. Our discovery that coral larvae can detect and respond to sound is the first description of an auditory response in the invertebrate phylum Cnidaria, which includes jellyfish, anemones, and hydroids as well as corals. If, like settlement-stage reef fish and crustaceans, coral larvae use reef noise as a cue for orientation, the alleviation of noise pollution in the marine environment may gain further urgency.Mark J. A. Vermeij, Kristen L. Marhaver, Chantal M. Huijbers, Ivan Nagelkerken and Stephen D. Simpso

The ecology of coral-microbe interactions

At every moment, a tropical reef coral interacts with millions of microbial organisms from tens of thousands of different species. Among these viruses, bacteria, archaea, dinoflagellates, and protists are cooperative symbionts as well as pathogens and parasites. Each interaction between a coral and a microscopic organism has ecological consequences for the coral community. In this dissertation, I show that juveniles of the Caribbean coral Montastraea faveolata suffer distance-dependent mortality in the presence of adult corals of the same species which is caused by microbial communities near these adults. This previously undiscovered structuring force will affect the spatial patterning of reefs and appears strong enough to drive the evolution of habitat selection behavior by coral larvae. The behavior of pre-settlement larvae differs based on both the microbial environment and the manner in which that environment is altered, indicating that water column microbes may be used as navigational information by dispersing corals. Sterilized seawater and penicillin both increase larval swimming rates, perhaps because larvae cannot detect the microbial "smell" of a suitable reef habitat, however only penicillin inhibits settlement and metamorphosis. Five antibiotics each induce a different pattern of abnormal behavior, indicating that the behavior of coral larvae could form the foundation of a new model system in toxicology. Furthermore, settlement failure on reefs may have a large behavioral component that has been underappreciated until now. The coral-dinoflagellate symbiosis is the best-known coral-microbe interaction however coral bleaching remains enigmatic. Based on observations made after a tropical storm, I propose that corals evolved bleaching as an adaptive mechanism to readjust symbiont communities after storm damage moves corallites into new light regimes. In a survey of viral diversity in the coral Diploria strigosa, I demonstrate that coral-associated viruses likely infect all other cells in the coral holobiont, including symbionts and potential pathogens. I propose that interactions among these viral groups could help to stabilize mutualistic coral-microbe interactions. Four additional natural history observations demonstrate the diversity of behaviors and interactions corals exhibit at the micron to millimeter scales and reveal that we have many more coral- microbe interactions left to discove

Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species

When juveniles must tolerate harsh environments early in life, the disproportionate success of certain phenotypes across multiple early life stages will dramatically influence adult community composition and dynamics. In many species, large offspring have a higher tolerance for stressful environments than do smaller conspecifics (parental effects). However, we have a poor understanding of whether the benefits of increased parental investment carry over after juveniles escape harsh environments or progress to later life stages (latent effects). To investigate whether parental effects and latent effects interactively influence offspring success, we determined the degree to which latent effects of harsh abiotic conditions are mediated by offspring size in two stony coral species. Larvae of both species were sorted by size class and exposed to relatively high-temperature or low-salinity conditions. Survivorship was quantified for six days in these stressful environments, after which surviving larvae were placed in ambient conditions and evaluated for their ability to settle and metamorphose. We subsequently assessed long-term post-settlement survival of one species in its natural environment. Following existing theory, we expected that, within and between species, larger offspring would have a higher tolerance for harsh environmental conditions than smaller offspring. We found that large size did enhance offspring performance in each species. However, large offspring size within a species did not reduce the proportional, negative latent effects of harsh larval environments. Furthermore, the coral species that produces larger offspring was more, not less, prone to negative latent effects. We conclude that, within species, large offspring size does not increase resistance to latent effects. Comparing between species, we conclude that larger offspring size does not inherently confer greater robustness, and we instead propose that other life history characteristics such as larval duration better predict the tolerance of offspring to harsh and variable abiotic conditions. Additionally, when considering how stressful environments influence offspring performance, studies that only evaluate direct effects may miss crucial downstream (latent) effects on juveniles that have significant consequences for long-term population dynamics

Appendix A. Parameter estimations and maximum-likelihood values for experiments depicted in Figs. 1–3.

Parameter estimations and maximum-likelihood values for experiments depicted in Figs. 1–3

Overview of the experimental setup.

<p>The position of coral larvae was observed in six Plexiglas tubes that were arranged around three central underwater loudspeakers to control for the effect of other factors that might influence the movement of larvae (e.g., currents, underwater light fields). Coral larvae are not drawn to scale.</p

Hartmann_etal_MEC_Fig_4_data

The behavioral responses of Orbicella faveolata larvae to photosymbiont infection with cells obtained from two cultured species and presented in Figure 4. The photosymbiont species include Breviolum minutum and Symbiodinium microadriaticum

Hartmann_etal_MEC_Fig_1_data

The gene expression data obtained from Orbicella faveolata larvae and used to generate Figure 1. The data matrix was filtered to only the genes that successfully hybridized (i.e., produced data) in at least three replicates for each treatment. Missing values were imputed and all values were normalized to a mean of zero and the same unit variance in each gene. The 'Name' column provides the gene annotation, if there is one. The subsequent columns contain data for the 20 samples. The sample names refer treatment group, which includes light status (L = Light, D = Dark), symbiont status (S = Symb, NS = NoSymb), and replicate number (1-5)

The experimental underwater sound field.

<p>Analysis of RMS power gradients on all three axes of the experimental set-up (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0010660#pone-0010660-g001" target="_blank">Figure 1</a>) during playback showed a 4.4 dB gradient within the chamber. Recordings were taken at three locations along the apparatus. The gradient in the measurements is near to a cylindrical model of geometric spreading (R_L = S_L – 10 log (R/R_ref)), as expected for shallow water environments, except that instead of a geometric model parameter of 10, the measured value was 11.1 (SEM = 1.4).</p