Farming behaviour of reef fishes increases the prevalence of coral disease associated microbes and black band disease.

Microbial community structure on coral reefs is strongly influenced by coral-algae interactions; however, the extent to which this influence is mediated by fishes is unknown. By excluding fleshy macroalgae, cultivating palatable filamentous algae and engaging in frequent aggression to protect resources, territorial damselfish (f. Pomacentridae), such as Stegastes, mediate macro-benthic dynamics on coral reefs and may significantly influence microbial communities. To elucidate how Stegastes apicalis and Stegastes nigricans may alter benthic microbial assemblages and coral health, we determined the benthic community composition (epilithic algal matrix and prokaryotes) and coral disease prevalence inside and outside of damselfish territories in the Great Barrier Reef, Australia. 16S rDNA sequencing revealed distinct bacterial communities associated with turf algae and a two to three times greater relative abundance of phylotypes with high sequence similarity to potential coral pathogens inside Stegastes's territories. These potentially pathogenic phylotypes (totalling 30.04% of the community) were found to have high sequence similarity to those amplified from black band disease (BBD) and disease affected corals worldwide. Disease surveys further revealed a significantly higher occurrence of BBD inside S. nigricans's territories. These findings demonstrate the first link between fish behaviour, reservoirs of potential coral disease pathogens and the prevalence of coral disease.

Intestinal microbiota in fishes: what's known and what's not.

High-throughput sequencing approaches have enabled characterizations of the community composition of numerous gut microbial communities, which in turn has enhanced interest in their diversity and functional relationships in different groups of vertebrates. Although fishes represent the greatest taxonomic and ecological diversity of vertebrates, our understanding of their gut microbiota and its functional significance has lagged well behind that of terrestrial vertebrates. In order to highlight emerging issues, we provide an overview of research on fish gut microbiotas and the biology of their hosts. We conclude that microbial community composition must be viewed within an informed context of host ecology and physiology, and that this is of particular importance with respect to research planning and sampling design.

Temperature-related variation in growth rate, size, maturation and life span in a marine herbivorous fish over a latitudinal gradient.

In ectotherms, growth rate, body size and maturation rate covary with temperature, with the direction and magnitude of variation predicted by the Temperature-Size Rule (TSR). Nutritional quality or availability of food, however, may vary over latitudinal gradients, resulting in ambiguous effects on body size and maturation rate. The Temperature-Constraint Hypothesis (TCH) predicts that marine herbivorous ectotherms are nutritionally compromised at latitudes exceeding 30°. This provides an opportunity to resolve the contrasting demographic responses of ectotherms to variation in temperature and nutritional status over latitudinal gradients. This study uses analysis of demographic rates to evaluate the predictions of the TSR in a marine herbivorous ectotherm sampled over a significant latitudinal gradient. The direction and magnitude of demographic variation was established in the marine herbivorous fish, Odax pullus (the butterfish), and compared with that of a phylogenetically related but trophically distinct species, the carnivorous Notolabrus fucicola (the banded wrasse). Both species were sampled at three locations across the length of New Zealand covering latitudes between 35°S and 49°S. Growth rate, mean size-at-age, age- and size-at-maturity, life span and abundance were estimated for each species at each location. Demographic traits of both taxa varied with latitude. Both species showed slower initial growth rates, and matured later at a larger body size at higher latitudes than populations sampled at lower latitudes. In addition, abundances increased significantly at higher latitudes in both species. These results were consistent with the TSR but not with the TCH, confirming that nutritional ecology (herbivore vs. carnivory) did not determine demographic patterns over a biologically significant latitudinal gradient. Results from this study suggest that the absence of herbivorous reef fishes from the higher latitudes of the Northern Hemisphere may not reflect a general physiological mechanism as suggested by the TCH and highlights the need to clarify the evolutionary histories of the marine biota of each hemisphere.

Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves.

The Great Barrier Reef (GBR) provides a globally significant demonstration of the effectiveness of large-scale networks of marine reserves in contributing to integrated, adaptive management. Comprehensive review of available evidence shows major, rapid benefits of no-take areas for targeted fish and sharks, in both reef and nonreef habitats, with potential benefits for fisheries as well as biodiversity conservation. Large, mobile species like sharks benefit less than smaller, site-attached fish. Critically, reserves also appear to benefit overall ecosystem health and resilience: outbreaks of coral-eating, crown-of-thorns starfish appear less frequent on no-take reefs, which consequently have higher abundance of coral, the very foundation of reef ecosystems. Effective marine reserves require regular review of compliance: fish abundances in no-entry zones suggest that even no-take zones may be significantly depleted due to poaching. Spatial analyses comparing zoning with seabed biodiversity or dugong distributions illustrate significant benefits from application of best-practice conservation principles in data-poor situations. Increases in the marine reserve network in 2004 affected fishers, but preliminary economic analysis suggests considerable net benefits, in terms of protecting environmental and tourism values. Relative to the revenue generated by reef tourism, current expenditure on protection is minor. Recent implementation of an Outlook Report provides regular, formal review of environmental condition and management and links to policy responses, key aspects of adaptive management. Given the major threat posed by climate change, the expanded network of marine reserves provides a critical and cost-effective contribution to enhancing the resilience of the Great Barrier Reef.

Intestinal Microbiome Richness of Coral Reef Damselfishes (Actinopterygii: Pomacentridae).

Fish gastro-intestinal system harbors diverse microbiomes that affect the host's digestion, nutrition, and immunity. Despite the great taxonomic diversity of fish, little is understood about fish microbiome and the factors that determine its structure and composition. Damselfish are important coral reef species that play pivotal roles in determining algae and coral population structures of reefs. Broadly, damselfish belong to either of two trophic guilds based on whether they are planktivorous or algae-farming. In this study, we used 16S rRNA gene sequencing to investigate the intestinal microbiome of 5 planktivorous and 5 algae-farming damselfish species (Pomacentridae) from the Great Barrier Reef. We detected Gammaproteobacteria ASVs belonging to the genus Actinobacillus in 80% of sampled individuals across the 2 trophic guilds, thus, bacteria in this genus can be considered possible core members of pomacentrid microbiomes. Algae-farming damselfish had greater bacterial alpha-diversity, a more diverse core microbiome and shared 35 ± 22 ASVs, whereas planktivorous species shared 7 ± 3 ASVs. Our data also highlight differences in microbiomes associated with both trophic guilds. For instance, algae-farming damselfish were enriched in Pasteurellaceae, whilst planktivorous damselfish in Vibrionaceae. Finally, we show shifts in bacterial community composition along the intestines. ASVs associated with the classes Bacteroidia, Clostridia, and Mollicutes bacteria were predominant in the anterior intestinal regions while Gammaproteobacteria abundance was higher in the stomach. Our results suggest that the richness of the intestinal bacterial communities of damselfish reflects host species diet and trophic guild.

O sistema gastro-intestinal de peixes abriga microbiomas diversos que afetam a digestão, nutrição e imunidade do hospedeiro. Apesar da grande diversidade taxonômica dos peixes, entende-se pouco sobre o microbioma dos peixes e fatores que determinam sua estrutura e composição. Peixes-donzela são espécies importantes em recifes de coral que exercem papéis pivotais na determinação da estrutura de algas e corais dos recifes. De forma geral, peixes-donzela pertencem à uma de duas guildas tróficas dependendo se são planctívoros ou algívoros. Nesse estudo, usamos sequenciamento do gene 16S rRNA para investigar o microbioma intestinal de cinco espécies planctívoras e cinco espécies algívoras de peixes-donzela (Pomacentridae) da Grande Barreira de Corais. Detectamos ASVs de Gammaproteobacteria pertencendo ao gênero Actinobacillus em 80% dos indivíduos amostrados nas duas guildas tróficas, logo, bactérias desse gênero podem ser consideradas como possíveis membros essenciais do microbioma dos pomacentrídeos. Peixes-donzela algívoros apresentaram uma maior alpha-diversidade bacteriana, um microbioma essencial mais diverso e compartilharam 35 ± 22 ASVs, e espécies planctívoras compartilharam 7 ± 3 ASVs. Nossos dados também ilustram diferenças nos microbiomas associados com ambas guildas tróficas. Por exemplo, peixes-donzela algívoros estavam enriquecidos em Pasteurellaceae, enquanto peixes-donzela planctívoros, em Vibrionaceae. Finalmente, demonstramos mudanças na composição da comunidade bacteriana associada com as classes Bacteroidia, Clostridia e Mollicutes foram predominantes nas regiões intestinais anteriores enquanto a abundância de Gammaproteobacteria foi maior no estômago. Nossos resultados sugerem que a riqueza das comunidades bacterianas intestinais de peixes-donzela refletem a dieta da espécie do hospedeiro, bem como a sua guilda trófica.

Extreme polyploidy in a large bacterium.

Cells rely on diffusion to move metabolites and biomolecules. Diffusion is highly efficient but only over short distances. Although eukaryotic cells have broken free of diffusion-dictated constraints on cell size, most bacteria and archaea are forced to remain small. Exceptions to this rule are found among the bacterial symbionts of surgeonfish; Epulopiscium spp. are cigar-shaped cells that reach lengths in excess of 600 mum. A large Epulopiscium contains thousands of times more DNA than a bacterium such as Escherichia coli, but the composition of this DNA is not well understood. Here, we present evidence that Epulopiscium contains tens of thousands of copies of its genome. Using quantitative, single-cell PCR assays targeting single-copy genes, we have determined that copy number is positively correlated with Epulopiscium cell size. Although other bacteria are known to possess multiple genomes, polyploidy of the magnitude observed in Epulopiscium is unprecedented. The arrangement of genomes around the cell periphery may permit regional responses to local stimuli, thus allowing Epulopiscium to maintain its unusually large size. Surveys of the sequences of single-copy genes (dnaA, recA, and ftsZ) revealed genetic homogeneity within a cell consistent with only a small amount ( approximately 1%) of the parental DNA being transferred to the next generation. The results also suggest that the abundance of genome copies in Epulopiscium may allow for an unstable genetic feature, a long mononucleotide tract, in an essential gene. With the evolution of extreme polyploidy and large cell size, Epulopiscium has acquired some of the advantages of eukaryotic cells.

Marine biology: Ageing a 'living fossil'.

A novel approach to determine the lifespan of an iconic fish, the coelacanth Latimeria chalumnae, reveals that they can live up to a hundred years. This re-focuses attention on the need to measure life-history traits that determine the demographics of fish populations.

Ongoing collapse of coral-reef shark populations.

Marine ecosystems are suffering severe depletion of apex predators worldwide; shark declines are principally due to conservative life-histories and fisheries overexploitation. On coral reefs, sharks are strongly interacting apex predators and play a key role in maintaining healthy reef ecosystems. Despite increasing fishing pressure, reef shark catches are rarely subject to specific limits, with management approaches typically depending upon no-take marine reserves to maintain populations. Here, we reveal that this approach is failing by documenting an ongoing collapse in two of the most abundant reef shark species on the Great Barrier Reef (Australia). We find an order of magnitude fewer sharks on fished reefs compared to no-entry management zones that encompass only 1% of reefs. No-take zones, which are more difficult to enforce than no-entry zones, offer almost no protection for shark populations. Population viability models of whitetip and gray reef sharks project ongoing steep declines in abundance of 7% and 17% per annum, respectively. These findings indicate that current management of no-take areas is inadequate for protecting reef sharks, even in one of the world's most-well-managed reef ecosystems. Further steps are urgently required for protecting this critical functional group from ecological extinction.

Recombination contributes to population diversification in the polyploid intestinal symbiont Epulopiscium sp. type B.

Epulopiscium sp. type B (Lachnospiraceae) is an exceptionally large, highly polyploid, intestinal symbiont of the coral reef dwelling surgeonfish Naso tonganus. These obligate anaerobes do not form mature endospores and reproduce solely through the production of multiple intracellular offspring. This likely makes them dependent on immediate transfer to a receptive host for dispersal. During reproduction, only a small proportion of Epulopiscium mother-cell DNA is inherited. To explore the impact of this unusual viviparous lifestyle on symbiont population dynamics, we investigated Epulopiscium sp. type B and their fish hosts collected over the course of two decades, at island and reef habitats near Lizard Island, Australia. Using multi-locus sequence analysis, we found that recombination plays an important role in maintaining diversity of these symbionts and yet populations exhibit linkage disequilibrium (LD). Symbiont populations showed spatial but not temporal partitioning. Surgeonfish are long-lived and capable of traveling long distances, yet the population structures of Epulopiscium suggest that adult fish tend to not roam beyond a limited locale. Codiversification analyses and traits of this partnership suggest that while symbionts are obligately dependent on their host, the host has a facultative association with Epulopiscium. We suggest that congression of unlinked markers contributes to LD estimates in this and other recombinant populations of bacteria. The findings here inform our understanding of evolutionary processes within intestinal Lachnospiraceae populations.

High population connectivity across the Indo-Pacific: Congruent lack of phylogeographic structure in three reef fish congeners.

We used the mitochondrial control region and a comparative approach to study the genetic population structure of two surgeonfishes, Naso brevirostris and Naso unicornis, across their Indo-central Pacific ranges. Our purpose was to compare our results with those of a previous study of Naso vlamingii [Klanten, S.O., van Herwerden, L., Choat J.H., 2007. Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar. Biol. 150, 659-670] another widely distributed Indo-central Pacific Naso species. We found no evidence of a barrier to gene flow between the Indian and Pacific Oceans for either species, consistent with what was shown for N. vlamingii. Overall, both target species lacked spatial population partitions and probably have complex patterns of gene flow on several spatial scales. Despite the lack of geographic population structure distinct clades were observed in N. brevirostris, similar to those found in N. vlamingii. Coalescence times for intraspecific clades of N. brevirostris and N. vlamingii approximate each other, suggesting parallel evolutionary histories. A bimodal mismatch distribution in N. brevirostris indicates that a biogeographic barrier separated N. brevirostris populations sometime during its species history. Naso unicornis, in contrast, lacked genetic structure of any kind, although it has what could represent a single surviving clade. Congruent lack of spatial population structure among all three species suggest that such patterns are not due to stochastic processes of DNA mutation and are most likely driven by ecological and environmental factors.

Geography and island geomorphology shape fish assemblage structure on isolated coral reef systems.

We quantify the relative importance of multi-scale drivers of reef fish assemblage structure on isolated coral reefs at the intersection of the Indian and Indo-Pacific biogeographical provinces. Large (>30 cm), functionally-important and commonly targeted species of fish, were surveyed on the outer reef crest/front at 38 coral reef sites spread across three oceanic coral reef systems (i.e. Christmas Island, Cocos (Keeling) Islands and the Rowley Shoals), in the tropical Indian Ocean (c. 1.126 x 106 km2). The effects of coral cover, exposure, fishing pressure, lagoon size and geographical context, on observed patterns of fish assemblage structure were modelled using Multivariate Regression Trees. Reef fish assemblages were clearly separated in space with geographical location explaining ~53 % of the observed variation. Lagoon size, within each isolated reef system was an equally effective proxy for explaining fish assemblage structure. Among local-scale variables, 'distance from port', a proxy for the influence of fishing, explained 5.2% of total variation and separated the four most isolated reefs from Cocos (Keeling) Island, from reefs with closer boating access. Other factors were not significant. Major divisions in assemblage structure were driven by sister taxa that displayed little geographical overlap between reef systems and low abundances of several species on Christmas Island corresponding to small lagoon habitats. Exclusion of geographical context from the analysis resulted in local processes explaining 47.3% of the variation, highlighting the importance of controlling for spatial correlation to understand the drivers of fish assemblage structure. Our results suggest reef fish assemblage structure on remote coral reef systems in the tropical eastern Indian Ocean reflects a biogeographical legacy of isolation between Indian and Pacific fish faunas and geomorphological variation within the region, more than local fishing pressure or reef condition. Our findings re-emphasise the importance that historical processes play in structuring contemporary biotic communities.

Cleaner fish drives local fish diversity on coral reefs.

Coral reefs are one of the most diverse habitats in the world, yet our understanding of the processes affecting their biodiversity is limited. At the local scale, cleaner fish are thought to have a disproportionate effect, in relation to their abundance and size, on the activity of many other fish species, but confirmation of this species' effect on local fish diversity has proved elusive. The cleaner fish Labroides dimidiatus has major effects on fish activity patterns and may indirectly affect fish demography through the removal of large numbers of parasites. Here we show that small reefs where L. dimidiatus had been experimentally excluded for 18 months had half the species diversity of fish and one-fourth the abundance of individuals. Only fish that move among reefs, however, were affected. These fish include large species that themselves can affect other reef organisms. In contrast, the distribution of resident fish was not affected by cleaner fish. Thus, many fish appear to choose reefs based on the presence of cleaner fish. Our findings indicate that a single small and not very abundant fish has a strong influence on the movement patterns, habitat choice, activity, and local diversity and abundance of a wide variety of reef fish species.

Patterns of lineage diversification in the genus Naso (Acanthuridae).

The evolutionary history of the reef fish genus Naso (F. Acanthuridae) was examined using a complete species-level molecular phylogeny of all recognized (19) species based on three loci (one nuclear ETS2 and two mitochondrial 16S, cyt b). This study demonstrates that distinct foraging modes and specialized body shapes arose independently at different times in the evolutionary history of the genus. Members of the subgenus Axinurus, characterized by a scombriform morphology, caudal fin structure and pelagic foraging mode, were consistently placed basal to the remaining Naso species, suggesting that pelagic foraging is plesiomorphic and benthic foraging derived in this genus. We used a genus-level phylogeny (nuclear marker, ETS2), which included several taxa from all other acanthurid genera, to obtain a range of age estimates for the most recent common ancestor of the genus Naso. These age estimates (range of 52-43.3 MY) were then used to estimate divergence times (by nonparametric rate smoothing method) of the node giving rise to extant Naso species using the combined sequence data (from all loci). The reconstruction of the pattern of divergence of extant species indicates two sequences of events. The basal species characterized by pelagic foraging modes arose during the Eocene and Oligocene. Most of the remaining Naso species, including those characterized by benthic foraging, arose over a period of 20 MY during the Miocene. Diversification during this period was associated with major plate tectonic and glaciation events, resulting in changes in sea level, ocean temperature and productivity regimes. Regardless of the foraging mode exhibited, all species of Naso have a caudal propulsive unit similar to that observed in pelagic scombriform fishes, a legacy of the basal position of the subgenus Axinurus in the phylogeny of the genus.