Ecological and biotechnological importance of secondary metabolites produced by coral-associated bacteria

Symbiotic relationships between corals and their associated micro-organisms are essential to maintain host homeostasis. Coral-associated bacteria (CAB) can have different beneficial roles in the coral metaorganism, such as metabolizing essential nutrients for the coral host and protecting the coral from pathogens. Many CAB exert these functions via secondary metabolites, which include antibacterial, antifouling, antitumour, antiparasitic and antiviral compounds. This review describes how analysis of CAB has led to the discovery of secondary metabolites with potential biotechnological applications. The most commonly found types of secondary metabolites, antimicrobial and antibiofilm compounds, are emphasized and described. Recently developed methods that can be applied to enhance the culturing of CAB from shallow-water reefs and the less-studied deep-sea coral reefs are also discussed. Last, we suggest how the combined use of meta-omics and innovative growth-diffusion techniques can vastly improve the discovery of novel compounds in coral environments.     

Fifty million years of herbivory on coral reefs: fossils,fish and functional innovations

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene–Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.     

High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef‐dwelling calcifier

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo‐West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological‐scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation.     

A new coral‐associated decapod assemblage from the Upper Miocene (Messinian) Upper Coralline Limestone of Malta (Central Mediterranean)

Abstract: A rich coral‐associated decapod assemblage is recorded from the ‘Depiru Beds’ of the upper part of the Upper Coralline Limestone (Messinian, Upper Miocene), from the island of Malta. Nineteen species within 17 genera have been discovered, where 14 genera are new for Malta. Four new species are described, namely Micippa annamariae sp. nov., Pilumnus scaber sp. nov., Panopeus muelleri sp. nov. and Herbstia melitense sp. nov. Herbstia melitense sp. nov. constitutes the first record of the genus from the fossil record in the Mediterranean region. This discovery more than doubles the number of known fossil decapod species from Malta. The fossil bivalve Jouannetia (J.) semicaudata Des Moulins, 1830 and the extant decapod Maja goltziana D’Oliveira, 1888, are also recorded for the first time from Malta. Other Neogene coral‐associated decapod assemblages are investigated and correlated with the new assemblage from Malta. The migration of taxa between the Mediterranean region and the Paratethys, particularly during the Lower Badenian (Langhian), is evidenced by the strong affinity of the Maltese decapod assemblage with that of the Middle Miocene Badenian assemblages from Hungary, Poland and Ukraine. Upper Miocene, Messinian assemblages from Spain, Algeria and Morocco are also similar to that from Malta.     

Similar regional effects among local habitats on the structure of tropical reef fish and coral communities

Aim We examined data on corals and reef fishes to determine how particular local habitat types contribute to variation in community structure across regions covering gradients in species richness and how consistent this was over time. Location Great Barrier Reef (GBR), Australia. Methods We compared large‐scale (1300 km), long‐term (11 years) data on fishes and corals that were collected annually at fixed sites in three habitats (inshore, mid‐shelf and outer‐shelf reefs) and six regions (latitudinal sectors) along a gradient of regional species richness in both communities. We used canonical approaches to partition variation in community structure (sites × species abundance data matrices) into components associated with habitat, region and time and Procrustes analyses to assess the degree of concordance between coral and fish community structure. Results Remarkably similar patterns emerged for both fish and coral communities occupying the same sites. Reefs that had similar coral communities also had similar fish communities. The fraction of the community data that could be explained by regional effects, independent of pure habitat effects, was similar in both fish (33%) and coral (36.9%) communities. Pure habitat effects were slightly greater in the fish (31.3%) than in the coral (20.1%) community. Time explained relatively little variation (fish = 7.9%, corals = 9.6%) compared with these two spatial factors. Conclusions Our results indicate either that fish and coral communities were structured in similar ways by processes associated with region, habitat and time, or that the variation in fish community structure tracked variation associated with the coral communities at these sites and thereby reflects an indirect link between the environment and the structure of fish communities mediated by corals. Irrespective of the causes of such commonality, we demonstrate that community structure, not just species richness, can be related to both habitat differences and regional setting simultaneously.     

Corallivory in tubelip wrasses: diet,feeding and trophic importance

This paper describes a 2 month study of the patterns of abundance, feeding pressure, diet and feeding selectivity in corallivorous tubelip wrasses (Labridae), rarely studied, yet widespread and abundant group of corallivores on Indo‐Pacific coral reefs. The relative abundance and feeding pressure of corallivorous wrasses and butterflyfishes (Chaetodontidae) in Kimbe Bay, Papua New Guinea, were compared. Overall, tubelip wrasses were more than twice as abundant as corallivorous butterflyfishes and accounted for three times as many feeding bites on corals. The three most abundant tubelip wrasses (yellowtail tubelip Diproctacanthus xanthurus, Allen's tubelip Labropsis alleni and the tubelip wrasse Labrichthys unilineatus) were all obligate corallivores taking > 97% of bites from the surface of live corals. Labropsis alleni and D. xanthurus were highly selective, consuming preferred prey species in proportions significantly higher than expected given their availability. In contrast, L. unilineatus was fairly non‐selective and consumed most corals in direct accordance with their availability. As coral predators, tubelip wrasses are highly comparable to coral‐feeding butterflyfishes in the coral species consumed, range of dietary specialization and their reliance on live coral. Tubelip wrasses, however, may supersede butterflyfishes as the predominant corallivorous family in some Indo‐Pacific locations, and coral‐feeding tubelip wrasses are likely to be severely affected by coral decline.     

Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef

Alpheid shrimp represent an abundant and diverse, but poorly characterized, component of the cryptic biodiversity of coral reefs worldwide. Sponge‐inhabiting alpheids provide a promising model system for exploring patterns of cryptic reef biodiversity because their habitats (hosts) are discrete and qualitatively distinct units. We tabulated data from 14 years of collections at Carrie Bow Cay, Belize to quantify patterns of diversity, host specificity, and dominance among sponge‐dwelling shrimp (Synalpheus), with special attention to eusocial species. From > 600 sampled sponges of 17 species, we recognized at least 36 Synalpheus shrimp species. Of these, 15 (42%) were new to science. Species accumulation curves suggest that we have sampled most of the Synalpheus diversity at Carrie Bow Cay. Diversity of sponge‐dwelling Synalpheus was slightly higher in shallow water, probably because of greater habitat diversity, than in deep water. Host specificity was surprisingly high, with > 50% of all shrimp species found in only a single sponge species each, although some shrimp species used as many as six hosts. Cohabitation of individual sponges by multiple shrimp species was rarer than expected by chance, supporting previous distributional and behavioural evidence that competition for hosts is strong and moulds patterns of host association. The fauna of most well‐sampled sponge species was dominated, both in numbers of individuals and in frequency of occurrence, by eusocial species. Eusocial shrimp species also inhabited a significantly greater number of sponge species than did non‐social shrimp. Consequently, > 65% of shrimp in our quantitative samples belonged to the four eusocial species, and on a per‐species basis, eusocial species were 17 times as abundant as non‐social species. Our data suggest that the highly diverse sponge‐dwelling shrimp assemblage of the Belize Barrier Reef is structured by competition, and that eusociality has allowed a small number of species to dominate the sponge resource.     

Environmental and geometric constraints on Indo-Pacific coral reef biodiversity

The Indo-Australian Archipelago supports the world's richest coral reef biodiversity hotspot. Traditional hypotheses that account for such exceptional biodiversity have highlighted the importance of environmental variables such as habitat area and energy input. Recently, however, an additional explanation has been proposed based on geometric constraints in the placement of geographical ranges within a bounded domain, which cause a mid-domain peak in species richness; the mid-domain effect (MDE). Here, for the first time, we examine the relative importance of area, energy and MDE jointly on species richness patterns. Model selection indicates that the best model incorporates MDE and reef area, but no energy effect; moreover, this best-fit model captures all major features of reef fish and coral species richness patterns. Habitat area is the major environmental factor influencing species richness. The prevention of further fragmentation and loss of habitat area is of critical importance for the conservation of coral reef biodiversity.     

Characterization of 16 microsatellite loci for a common coral reef fish,the fierce shrimpgoby Ctenogobiops feroculus

We developed 16 pairs of primers for microsatellite loci of the fierce shrimpgoby, Ctenogobiops feroculus. Analysis of 35–40 gobies per locus from five islands in French Polynesia indicated that allele frequency varied from two to 30 per locus, while observed heterozygosity ranged between 0.05 and 0.98. These microsatellites should provide insight into patterns of dispersal and connectivity among populations of this common coral reef fish.     

Six microsatellite loci from the deep‐sea coral Corallium lauuense (Octocorallia: Coralliidae) from the islands and seamounts of the Hawaiian archipelago

Gorgonian octocorals are among the dominant deep‐sea benthic taxa of many seamounts. Seamount fauna are threatened by destructive fisheries practices, yet little is known about the physical and biological processes that maintain species on seamounts. Few informative molecular markers have been found in deep‐water corals or in gorgonian octocorals. Here we report the characterization of six highly polymorphic microsatellite loci for the deep‐sea precious coral Corallium lauuense from Hawaii using enriched genomic DNA libraries. These loci are being used to examine gene flow and stock structure among seamount and island populations to better understand dispersal and connectivity of seamount species.