Mark J. A. Vermeij

Surviving in a Marine Desert: The Sponge Loop Retains Resources Within Coral Reefs

Sponge Pump “Darwins Paradox” asks how productive and diverse ecosystems like coral reefs thrive in the marine equivalent of a desert. De Goeij et al. (p. 108) now show that coral reef sponges are part of a highly efficient recycling pathway for dissolved organic matter (DOM), converting it, via rapid sponge-cell turnover, into cellular detritus that becomes food for reef consumers. DOM transfer through the sponge loop approaches the gross primary production rates required for the entire coral reef ecosystem. Sponges take up dissolved organic matter and convert it into consumable cellular material. Ever since Darwin’s early descriptions of coral reefs, scientists have debated how one of the world’s most productive and diverse ecosystems can thrive in the marine equivalent of a desert. It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna. This “sponge loop” was confirmed in aquarium and in situ food web experiments, using 13C- and 15N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as coral reefs persist in oligotrophic seas—the reef’s paradox—and has implications for reef ecosystem functioning and conservation strategies.

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.

Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow

Understanding patterns of connectivity among populations of marine organisms is essential for the development of realistic, spatially explicit models of population dynamics. Two approaches, empirical genetic patterns and oceanographic dispersal modelling, have been used to estimate levels of evolutionary connectivity among marine populations but rarely have their potentially complementary insights been combined. Here, a spatially realistic Lagrangian model of larval dispersal and a theoretical genetic model are integrated with the most extensive study of gene flow in a Caribbean marine organism. The 871 genets collected from 26 sites spread over the wider Caribbean subsampled 45.8% of the 1900 potential unique genets in the model. At a coarse scale, significant consensus between modelled estimates of genetic structure and empirical genetic data for populations of the reef‐building coral Montastraea annularis is observed. However, modelled and empirical data differ in their estimates of connectivity among northern Mesoamerican reefs indicating that processes other than dispersal may dominate here. Further, the geographic location and porosity of the previously described east–west barrier to gene flow in the Caribbean is refined. A multi‐prong approach, integrating genetic data and spatially realistic models of larval dispersal and genetic projection, provides complementary insights into the processes underpinning population connectivity in marine invertebrates on evolutionary timescales.

Lytic to temperate switching of viral communities

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’.

Survival and settlement success of coral planulae: Independent and synergistic effects of macroalgae and microbes

Restoration of degraded coral reef communities is dependent on successful recruitment and survival of new coral planulae. Degraded reefs are often characterized by high cover of fleshy algae and high microbial densities, complemented by low abundance of coral and coral recruits. Here, we investigated how the presence and abundance of macroalgae and microbes affected recruitment success of a common Hawaiian coral. We found that the presence of algae reduced survivorship and settlement success of planulae. With the addition of the broad-spectrum antibiotic, ampicillin, these negative effects were reversed, suggesting that algae indirectly cause planular mortality by enhancing microbial concentrations or by weakening the coral’s resistance to microbial infections. Algae further reduced recruitment success of corals as planulae preferentially settled on algal surfaces, but later suffered 100% mortality. In contrast to survival, settlement was unsuccessful in treatments containing antibiotics, suggesting that benthic microbes may be necessary to induce settlement. These experiments highlight potential complex interactions that govern the relationships between microbes, algae and corals and emphasize the importance of microbial dynamics in coral reef ecology and restoration.

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae.

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral–CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs.

Morphogenesis of the branching reef coral Madracis mirabilis

Understanding external deciding factors in growth and morphology of reef corals is essential to elucidate the role of corals in marine ecosystems, and to explain their susceptibility to pollution and global climate change. Here, we extend on a previously presented model for simulating the growth and form of a branching coral and we compare the simulated morphologies to three–dimensional (3D) images of the coral species Madracis mirabilis. Simulation experiments and isotope analyses of M. mirabilis skeletons indicate that external gradients of dissolved inorganic carbon (DIC) determine the morphogenesis of branching, phototrophic corals. In the simulations we use a first principle model of accretive growth based on local interactions between the polyps. The only species–specific information in the model is the average size of a polyp. From flow tank and simulation studies it is known that a relatively large stagnant and diffusion dominated region develops within a branching colony. We have used this information by assuming in our model that growth is entirely driven by a diffusion–limited process, where DIC supply represents the limiting factor. With such model constraints it is possible to generate morphologies that are virtually indistinguishable from the 3D images of the actual colonies.

Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors

Significance Microbial communities associated with coral reefs influence the health and sustenance of keystone benthic organisms (e.g., coral holobionts). The present study investigated the community structure and metabolic potential of microbes inhabiting coral reefs located across an extensive area in the central Pacific. We found that the taxa present correlated strongly with the percent coverage of corals and algae, while community metabolic potential correlated best with geographic location. These findings are inconsistent with prevailing biogeographic models of microbial diversity (e.g., distance decay) and metabolic potential (i.e., similar functional profiles regardless of phylogenetic variability). Based on these findings, we propose that the primary carbon sources determine community structure and that local biogeochemistry determines finer-scale metabolic function. Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.

Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC).

Coral-excavating sponges are the most important bioeroders on Caribbean reefs and increase in abundance throughout the region. This increase is commonly attributed to a concomitant increase in food availability due to eutrophication and pollution. We therefore investigated the uptake of organic matter by the two coral-excavating sponges Siphonodictyon sp. and Cliona delitrix and tested whether they are capable of consuming dissolved organic carbon (DOC) as part of their diet. A device for simultaneous sampling of water inhaled and exhaled by the sponges was used to directly measure the removal of DOC and bacteria in situ. During a single passage through their filtration system 14% and 13% respectively of the total organic carbon (TOC) in the inhaled water was removed by the sponges. 82% (Siphonodictyon sp.; mean±SD; 13±17 μmol L−1) and 76% (C. delitrix; 10±12 μmol L−1) of the carbon removed was taken up in form of DOC, whereas the remainder was taken up in the form of particulate organic carbon (POC; bacteria and phytoplankton) despite high bacteria retention efficiency (72±15% and 87±10%). Siphonodictyon sp. and C. delitrix removed DOC at a rate of 461±773 and 354±562 μmol C h−1 respectively. Bacteria removal was 1.8±0.9×1010 and 1.7±0.6×1010 cells h−1, which equals a carbon uptake of 46.0±21.2 and 42.5±14.0 μmol C h−1 respectively. Therefore, DOC represents 83 and 81% of the TOC taken up by Siphonodictyon sp. and C. delitrix per hour. These findings suggest that similar to various reef sponges coral-excavating sponges also mainly rely on DOC to meet their carbon demand. We hypothesize that excavating sponges may also benefit from an increasing production of more labile algal-derived DOC (as compared to coral-derived DOC) on reefs as a result of the ongoing coral-algal phase shift.

Stable and sporadic symbiotic communities of coral and algal holobionts

Coral and algal holobionts are assemblages of macroorganisms and microorganisms, including viruses, Bacteria, Archaea, protists and fungi. Despite a decade of research, it remains unclear whether these associations are spatial–temporally stable or species-specific. We hypothesized that conflicting interpretations of the data arise from high noise associated with sporadic microbial symbionts overwhelming signatures of stable holobiont members. To test this hypothesis, the bacterial communities associated with three coral species (Acropora rosaria, Acropora hyacinthus and Porites lutea) and two algal guilds (crustose coralline algae and turf algae) from 131 samples were analyzed using a novel statistical approach termed the Abundance-Ubiquity (AU) test. The AU test determines whether a given bacterial species would be present given additional sampling effort (that is, stable) versus those species that are sporadically associated with a sample. Using the AU test, we show that coral and algal holobionts have a high-diversity group of stable symbionts. Stable symbionts are not exclusive to one species of coral or algae. No single bacterial species was ubiquitously associated with one host, showing that there is not strict heredity of the microbiome. In addition to the stable symbionts, there was a low-diversity community of sporadic symbionts whose abundance varied widely across individual holobionts of the same species. Identification of these two symbiont communities supports the holobiont model and calls into question the hologenome theory of evolution.