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

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

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

Juvenile corals inherit mutations acquired during the parents lifespan

128 years ago, August Weismann proposed that the only source of inherited genetic variation in animals is the germline. Julian Huxley reasoned that if this were true, it would falsify Jean-Baptiste Lamarck′s theory that acquired characteristics are heritable. Since then, scientists have discovered that not all animals segregate germline cells from somatic cells permanently and early in development. In fact, throughout their lives, Cnidaria and Porifera maintain primordial stem cells that continuously give rise to both germline and somatic cells. The fate of mutations generated in this primordial stem cell line during adulthood remains an open question. It was unknown whether post−embryonic mutations could be heritable in animals−until now. Here we use two independent genetic marker analyses to show that post-embryonic mutations are inherited in the coral Acropora palmata (Cnidaria, Anthozoa). This discovery upends the long-held supposition that post-embryonic genetic mutations acquired over an animal′s lifetime in non-germline tissues are not heritable2. Over the centuries-long lifespan of a coral, the inheritance of post-embryonic mutations may not only change allele frequencies in the local larval pool but may also spread novel alleles across great distances via larval dispersal. Thus, corals may have the potential to adapt to changing environments via heritable somatic mutations. This mechanism challenges our understanding of animal adaptation and prompts a deeper examination of both the process of germline determination in clonal animals and the role of post−embryonic genetic mutations in adaptation and epigenetics. Understanding the role of post−embryonic mutations in animal adaptation will be crucial as ecological change accelerates in the Anthropocene

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

Movement of coral larvae towards reef sounds.

<p>(A) The proportion of coral larvae at various distances from speakers playing reef sounds are given as averages of Day 1 and 2 of the experiment (+1SEM). (B) Proportion of larvae at each distance class that were observed against the upper surface of the chambers (i.e., the surface nearest the speakers) when reef sounds were played from above (blue) and sounds were played from aside (light blue). Data are shown as averages from Day 3 of the experiment (+1SEM).</p

Engineered Substrates Reveal Species-Specific Inorganic Cues for Coral Larval Settlement

The widespread loss of stony reef-building coral populations has been compounded by pervasive recruitment failure, i.e., the low or absent settlement and survival of coral juveniles. To combat global coral reef stressors and rebuild coral communities, restoration practitioners have developed workflows to rear and settle vulnerable coral larvae in the laboratory and subsequently outplant settled juveniles back to natural and artificial reefs. These workflows often make use of the natural biochemical settlement cues present in crustose coralline algae (CCA), which can be presented to swimming larvae as extracts, fragments, or live algal sheets to induce settlement. In this work, we investigated the potential for inorganic chemical cues to complement these known biochemical effects. We designed settlement substrates made from lime mortar (CaCO3) and varied their composition with the use of synthetic and mineral additives, including sands, glasses, and alkaline earth carbonates. In experiments with larvae of two Caribbean coral species, Acropora palmata (elkhorn coral) and Diploria labyrinthiformis (grooved brain coral), we saw additive-specific settlement preferences (>10-fold settlement increase) in the absence of any external biochemical cues. Interestingly, these settlement trends were independent of bulk surface properties such as surface roughness and wettability. Instead, our results suggest that not only can settling coral larvae sense and positively respond to soluble inorganic materials, but that they can also detect localized topographical features more than an order of magnitude smaller than their body width. Our findings open a new area of research in coral reef restoration, in which engineered substrates can be designed with a combination of organic and inorganic additives to increase larval settlement, and perhaps also improve post-settlement growth, mineralization, and defense

Millimeter-scale ridges increase the duration of larval settling windows.

(a) Visualization of the relative fluid speed over flat (left) and ridged (right) substrates during peak (top) and turning point (bottom) flow. The fluid velocity (U) is normalized by the average larval swimming velocity (uℓ). Dotted black boxes represent regions ≤1.5 mm above the substrate surface that were used to calculate duration of settlement windows. Black arrows near the bottoms of the ridges indicate regions where the velocity remains low even at the turning points. (b) The average relative flow speed within the dotted black regions plotted over an average period for flat (top) and ridged (bottom) substrates. The yellow regions highlight the settling windows during which the local flow speed drops below uℓ (black line) plus one standard deviation (grey band).</p