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 of 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 sporadice 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

Restoration of critically endangered elkhorn coral (Acropora palmata) populations using larvae reared from wild-caught gametes

AbstractElkhorn coral (Acropora palmata) populations provide important ecological functions on shallow Caribbean reefs, many of which were lost when a disease reduced their abundance by more than 95% beginning in the mid-1970s. Since then, a lack of significant recovery has prompted rehabilitation initiatives throughout the Caribbean. Here, we report the first successful outplanting and long-term survival of A. palmata settlers reared from gametes collected in the field. A. palmata larvae were settled on clay substrates (substrate units) and either outplanted on the reef two weeks after settlement or kept in a land-based nursery. After 2.5 years, the survival rate of A. palmata settlers outplanted two weeks after settlement was 6.8 times higher (3.4%) than that of settlers kept in a land-based nursery (0.5%). Furthermore, 32% of the substrate units on the reef still harbored one or more well-developed recruit compared to 3% for substrate units kept in the nursery. In addition to increasing survival, outplanting A. palmata settlers shortly after settlement reduced the costs to produce at least one 2.5-year-old A. palmata individual from $325 to$13 USD. Thus, this study not only highlights the first successful long-term rearing of this critically endangered coral species, but also shows that early outplanting of sexually reared coral settlers can be more cost-effective than the traditional approach of nursery rearing for restoration efforts aimed at rehabilitating coral populations

Natural History of Coral-Algae Competition across a Gradient of Human Activity in the Line Islands

Competition between corals and benthic algae is prevalent on coral reefs worldwide and has the potential to influence the structure of the reef benthos. Human activities may influence the outcome of these interactions by favoring algae to become the superior competitor, and this type of change in competitive dynamics is a potential mechanism driving coral-algal phase shifts. Here we surveyed the types and outcomes of coral-algal interactions varied across reefs on the different islands. On reefs surrounding inhabited islands, however, turf algae were generally the superior competitors. When corals were broken down by size class, we found that the smallest and the largest coral colonies were the best competitors against algae; the former successfully fought off algae while being completely surrounded, and the latter generally avoided algal overgrowth by growing up above the benthos. Our data suggest that human disruption of the reef ecosystem may lead to a building pattern of competitive disadvantage for corals against encroaching algae, potentially initiating a transition towards algal dominance

Non-native coral species dominate the fouling community on a semi-submersible platform in the southern Caribbean

A coral community was examined on a semi-submersible platform that was moored at the leeward side of Curaçao, in the southern Caribbean, from August 2016 until August 2017. This community included several non-native or cryptogenic species. Among them were two scleractinian corals (Tubastraea coccinea and T. tagusensis) and two octocorals (Chromonephthea sp. and an unidentified Nephtheidae sp.). This is the first reported presence of T. tagusensis in the southern Caribbean, and the genus Chromonephthea in the Caribbean region. An ascidian, Perophora cf. regina, is also reported from the southern Caribbean for the first time, as well as a coral-associated vermetid gastropod, Petaloconchus sp., first recorded in the Caribbean in 2014. Lack of biofouling management could potentially harm indigenous marine fauna through the introduction of non-native species. Therefore monitoring communities associated with semi-submersible platforms is essential to track the presence and dispersal of non-native, potentially invasive species

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

Local Genomic Adaptation of Coral Reef-Associated Microbiomes to Gradients of Natural Variability and Anthropogenic Stressors

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 transger 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)

7 pages, 3 figures, 2 tablesCoral-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 mmol 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. © 2014 Mueller et al.The research leading to these results has received funding from the European Union Seventh Framework Programme (P7/2007-2013) under grant agreement no 244161 (Future of Reefs in a Changing Environment) and the Innovational Research Incentives Scheme of the Netherlands Organization for Scientific Research (NWO-VENI; 863.10.009; pers. grant to JMdG)Peer Reviewe

Data used to assess historical changes (1905-present) in catch size and composition reflecting altering fisheries practices on a small Caribbean island

Effective assessments of the status of Caribbean fish communities require historical baselines to adequately understand how much fish communities have changed through time. To identify such changes and their causes, we compiled a historical overview using data collected at the beginning (1905-1908), middle (1958-1965) and end (1984-2016) of the 20th century, of the artisanal fishing practices and their effects on fish populations around Curaçao, a small island in the southern Caribbean. We documented historical trends in total catch, species composition, and catch sizes per fisher per month for different types of fisheries and related these to technological and environmental changes affecting the island’s fisheries and fish communities. We found that since 1905, fishers targeted species increasingly farther from shore after species occurring closer to shore had become rare. This resulted in surprisingly similar catches in terms of weight, but not composition. Large predatory reef fishes living close to shore (e.g., large Epinephelid species) had virtually disappeared from catches around the mid-20th century, questioning the use of data from this period as baseline data for modern day fish assessments. Secondly, we compared fish landings to in-situ counts from 1969 to estimate the relative contributions of habitat destruction and overfishing to the changes in fish abundance around Curaçao. The decline in coral dominated reef communities corresponded to a concurrent decrease in the abundance and diversity of smaller reef fish species not targeted by fishers, suggesting habitat loss, in addition to fishing, caused the observed declines in reef fish abundance around Curaçao

Historical changes (1905-present) in catch size and composition reflect altering fisheries practices on a small Caribbean island

Effective assessments of the status of Caribbean fish communities require historical baselines to adequately understand how much fish communities have changed through time. To identify such changes and their causes, we compiled a historical overview using data collected at the beginning (1905-1908), middle (1958-1965) and end (1984-2016) of the 20th century, of the artisanal fishing practices and their effects on fish populations around Curaçao, a small island in the southern Caribbean. We documented historical trends in total catch, species composition, and catch sizes per fisher per month for different types of fisheries and related these to technological and environmental changes affecting the island's fisheries and fish communities. We found that since 1905, fishers targeted species increasingly farther from shore after species occurring closer to shore had become rare. This resulted in surprisingly similar catches in terms of weight, but not composition. Large predatory reef fishes living close to shore (e.g., large Epinephelid species) had virtually disappeared from catches around the mid-20th century, questioning the use of data from this period as baseline data for modern day fish assessments. Secondly, we compared fish landings to in-situ counts from 1969 to estimate the relative contributions of habitat destruction and overfishing to the changes in fish abundance around Curaçao. The decline in coral dominated reef communities corresponded to a concurrent decrease in the abundance and diversity of smaller reef fish species not targeted by fishers, suggesting habitat loss, in addition to fishing, caused the observed declines in reef fish abundance around Curaçao.</p