Decline of a distinct coral reef holobiont community under ocean acidification.

BACKGROUND: Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH - an important global coral reef stressor - can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. RESULTS: We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. CONCLUSIONS: We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. Video Abstract.

Effects of low pH on the coral reef cryptic invertebrate communities near CO2 vents in Papua New Guinea.

Small cryptic invertebrates (the cryptofauna) are extremely abundant, ecologically important, and species rich on coral reefs. Ongoing ocean acidification is likely to have both direct effects on the biology of these organisms, as well as indirect effects through cascading impacts on their habitats and trophic relationships. Naturally acidified habitats have been important model systems for studying these complex interactions because entire communities that are adapted to these environmental conditions can be analyzed. However, few studies have examined the cryptofauna because they are difficult to census quantitatively in topographically complex habitats and are challenging to identify. We addressed these challenges by using Autonomous Reef Monitoring Structures (ARMS) for sampling reef-dwelling invertebrates >2 mm in size and by using DNA barcoding for taxonomic identifications. The study took place in Papua New Guinea at two reef localities, each with three sites at varying distances from carbon dioxide seeps, thereby sampling across a natural gradient in acidification. We observed sharp overall declines in both the abundance (34-56%) and diversity (42-45%) of organisms in ARMS under the lowest pH conditions sampled (7.64-7.75). However, the overall abundance of gastropods increased slightly in lower pH conditions, and crustacean and gastropod families exhibited varying patterns. There was also variability in response between the two localities, despite their close proximity, as one control pH site displayed unusually low diversity and abundances for all invertebrate groups. The data illustrate the complexity of responses of the reef fauna to pH conditions, and the role of additional factors that influence the diversity and abundance of cryptic reef invertebrates.

Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea.

High-throughput sequencing (HTS) of DNA barcodes (metabarcoding), particularly when combined with standardized sampling protocols, is one of the most promising approaches for censusing overlooked cryptic invertebrate communities. We present biodiversity estimates based on sequencing of the cytochrome c oxidase subunit 1 (COI) gene for coral reefs of the Gulf of Aqaba, a semi-enclosed system in the northern Red Sea. Samples were obtained from standardized sampling devices (Autonomous Reef Monitoring Structures (ARMS)) deployed for 18 months. DNA barcoding of non-sessile specimens >2 mm revealed 83 OTUs in six phyla, of which only 25% matched a reference sequence in public databases. Metabarcoding of the 2 mm - 500 µm and sessile bulk fractions revealed 1197 OTUs in 15 animal phyla, of which only 4.9% matched reference barcodes. These results highlight the scarcity of COI data for cryptobenthic organisms of the Red Sea. Compared with data obtained using similar methods, our results suggest that Gulf of Aqaba reefs are less diverse than two Pacific coral reefs but much more diverse than an Atlantic oyster reef at a similar latitude. The standardized approaches used here show promise for establishing baseline data on biodiversity, monitoring the impacts of environmental change, and quantifying patterns of diversity at regional and global scales.

Commonness and rarity in the marine biosphere.

Explaining patterns of commonness and rarity is fundamental for understanding and managing biodiversity. Consequently, a key test of biodiversity theory has been how well ecological models reproduce empirical distributions of species abundances. However, ecological models with very different assumptions can predict similar species abundance distributions, whereas models with similar assumptions may generate very different predictions. This complicates inferring processes driving community structure from model fits to data. Here, we use an approximation that captures common features of "neutral" biodiversity models--which assume ecological equivalence of species--to test whether neutrality is consistent with patterns of commonness and rarity in the marine biosphere. We do this by analyzing 1,185 species abundance distributions from 14 marine ecosystems ranging from intertidal habitats to abyssal depths, and from the tropics to polar regions. Neutrality performs substantially worse than a classical nonneutral alternative: empirical data consistently show greater heterogeneity of species abundances than expected under neutrality. Poor performance of neutral theory is driven by its consistent inability to capture the dominance of the communities' most-abundant species. Previous tests showing poor performance of a neutral model for a particular system often have been followed by controversy about whether an alternative formulation of neutral theory could explain the data after all. However, our approach focuses on common features of neutral models, revealing discrepancies with a broad range of empirical abundance distributions. These findings highlight the need for biodiversity theory in which ecological differences among species, such as niche differences and demographic trade-offs, play a central role.

The diversity of coral reefs: what are we missing?

Tropical reefs shelter one quarter to one third of all marine species but one third of the coral species that construct reefs are now at risk of extinction. Because traditional methods for assessing reef diversity are extremely time consuming, taxonomic expertise for many groups is lacking, and marine organisms are thought to be less vulnerable to extinction, most discussions of reef conservation focus on maintenance of ecosystem services rather than biodiversity loss. In this study involving the three major oceans with reef growth, we provide new biodiversity estimates based on quantitative sampling and DNA barcoding. We focus on crustaceans, which are the second most diverse group of marine metazoans. We show exceptionally high numbers of crustacean species associated with coral reefs relative to sampling effort (525 species from a combined, globally distributed sample area of 6.3 m(2)). The high prevalence of rare species (38% encountered only once), the low level of spatial overlap (81% found in only one locality) and the biogeographic patterns of diversity detected (Indo-West Pacific>Central Pacific>Caribbean) are consistent with results from traditional survey methods, making this approach a reliable and efficient method for assessing and monitoring biodiversity. The finding of such large numbers of species in a small total area suggests that coral reef diversity is seriously under-detected using traditional survey methods, and by implication, underestimated.

Mitochondrial DNA variation of a natural population of Gyrodactylus thymalli (Monogenea) from the type locality River Hnilec, Slovakia.

The monogenean flatworm Gyrodactylus thymalli (Zitnan, Helminthologia, 2:266-269, 1960) is considered a harmless ectoparasite on grayling (Thymallus thymallus). The species is closely related to G. salaris Malmberg, 1957 that causes severe gyrodactylosis on Atlantic salmon (Salmo salar) in many Norwegian rivers. In this paper, we study the mitochondrial diversity of a G. thymalli population from one of the type localities Hrable on River Hnilec, Slovakia. By sequencing parts of the mitochondrial NADH dehydrogenase subunit 5 gene, we detected three haplotypes that differ from each other by 2.1-4.1%. The haplotype HnilecI was found most common. Our data suggest that River Hnilec has been colonized independently at least three times with G. thymalli.

The complete mitochondrial DNA sequence of the monogenean Gyrodactylus thymalli (Platyhelminthes: Monogenea), a parasite of grayling (Thymallus thymallus).

We present the complete mitochondrial (mt) genome of Gyrodactylus thymalli, a monogenean ectoparasite on grayling (Thymallus thymallus). The circular genome is 14788 bp in size and includes all 35 genes recognized from other flatworm mt genomes. The overall A+T content of the mt genome is 62.8%. Twenty regions of non-coding DNA ranging from 1 to 111 bp in length were identified in addition to 2 highly conserved large non-coding regions 799 bp and 767 bp in size. Compared to the recently described mt DNA of the closely related G. salaris from Atlantic salmon from Signaldalselva, Norway, the mitochondrial genome of G. thymalli from Hnilec, Slovakia, differs on average by 2.2%.

Dactylogyrids (Platyhelminthes: Monogenoidea) parasitizing butterfly fishes (Teleostei: Chaetodontidae) from the coral reefs of Palau, Moorea, Wallis, New Caledonia, and Australia: species of Euryhaliotrematoides n. gen. and Aliatrema n. gen.

Seven species of Euryhaliotrematoides n. gen. and 1 species of Aliatrema n. gen. (Monogenoidea; Dactylogyridae) are described and reported from the gills of 15 species of butterfly fishes (Chaetodontidae) from the coral reefs of Moorea (French Polynesia), Wallis (Wallis and Futuna), Heron and Lizard (Australia), Palau (Micronesia), and New Caledonia: Aliatrema cribbi n. sp. from Chaetodon auriga, Chaetodon lunula, Chaetodon trifasciatus, Chaetodon ulietensis, Chaetodon vagabundus, Forcipiger flavisissimus, and Heniochus chrysostomus; Euryhaliotrematoides annulocirrus n. comb. from C. auriga, C. lunula, and C. vagabundus; Euryhaliotrematoides aspistis n. sp. from C. auriga, Chaetodon citrinellus, C. lunula, Chaetodon reticulatus, C. ulietensis, and C. vagabundus; Euryhaliotrematoides berenguelae n. sp. from C. citrinellus, Chaetodon ornatissimus, and F. flavisissimus; Euryhaliotrematoides grandis n. comb. from C. auriga, C. citrinellus, Chaetodon ephippium, Chaetodon kleinii, Chaetodon lineolatus, C. lunula, C. ornatissimus, C. trifasciatus, C. vagabundus, and H. chrysostomus; Euryhaliotrematoides microphallus n. comb. from C. auriga, C. citrinellus, C. ephippium, C. kleinii, C. lunula, C. ornatissimus, C. reticulatus, Chaetodon trifascialis, C. trifasciatus, C. vagabundus, F. flavisissimus, and H. chrysostomus; Euryhaliotrematoides pirulum n. sp. from C. auriga, C. citrinellus, C. lunula, C. trifasciatus, and C. vagabundus; and Euryhaliotrematoides triangulovagina n. comb. from C. auriga, C. citrinellus, C. kleinii, C. lunula, C. ornatissimus, C. vagabundus, F. flavisissimus, H. chrysostomus, and Hemitaurichthys polylepis. All reports of previously described species are new locality records. With exceptions of E. grandis and E. annulocirrus on C. auriga and C. lunula and E. triangulovagina and E. microphallus on C. auriga, all reports are new host records. Haliotrema hainanensis and H. affinis are considered junior subjective synonyms of E. triangulovagina and E. annulocirrus, respectively. Aliatrema n. gen. is characterized by marine dactylogyrids with tandem gonads (germarium pretesticular), haptoral hooks with upright acute thumbs, a coiled copulatory organ with counterclockwise rings and funnel-shaped base but lacking an accessory piece, and a dextral vaginal pore. Euryhaliotrematoides n. gen. is characterized by marine dactylogyrids having tandem gonads (germarium pretesticular), haptoral hooks with upright acute thumbs, a coiled copulatory organ with counterclockwise rings and funnel-shaped base, a vas deferens looping the left intestinal cecum, and a dextral vaginal pore.

Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parasitizing butterfly fishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean.

Haliotrema species are described and/or reported from the gills of butterfly fishes (Chaetodontidae) from coral reefs of the Indo-West Pacific islands: Moorea (French Polynesia), Palau (Micronesia), Wallis (Wallis and Futuna), New Caledonia, Lizard Island and Heron Island (Great Barrier Reef, Australia). Haliotrema angelopterum sp. nov., a new species of Monogenoidea parasite from seven species of Chaetodon Linnaeus, 1758 (Chaetodontidae), is described. A new redescription and statute are given for Haliotrema aurigae (Yamaguti, 1968) comb. nov., a parasite from ten species of Chaetodon and one species of Heniochus Cuvier, 1816 (Chaetodontidae). New records of Haliotrema scyphovagina Yamaguti, 1968 are reported from two localities and from several host species belonging to the genera Chaetodon and Forcipiger Jordan and McGregor, 1898 (Chaetodontidae).

Recognition of two genetic groups in the Klebsiella oxytoca taxon on the basis of chromosomal beta-lactamase and housekeeping gene sequences as well as ERIC-1 R PCR typing.

Whilst searching for a molecular method to identify the different species of Raoultella and Klebsiella oxytoca, it was observed that the OXY-1 and OXY-2 beta-lactamase-producing K. oxytoca isolates displayed two distinguishable enterobacterial repetitive intergenic consensus (ERIC)-1R profiles. It was hypothesized that the two groups of chromosomal beta-lactamases might correspond to two groups of strains in the K. oxytoca taxon. To confirm this hypothesis, clinical isolates and reference strains of K. oxytoca were studied by determination of the sequence of their bla(OXY) genes, and of a partial fragment of their 16S rRNA (387 bp) and rpoB (512 bp) genes. The sequence data were phylogenetically analysed by using the parsimony method. Four clinical isolates possessed a bla(OXY-1) gene and nine possessed a bla(OXY-2) gene. The mean percentage of rpoB and 16S rRNA gene identity was > 99% within each group of strains, whereas it was 96.56 +/- 0.24% for rpoB genes and 97.80 +/- 0.22% for 16S rRNA genes between the group of strains harbouring the bla(OXY-1) gene and the group harbouring the bla(OXY-2) gene. The phylogenetic tree resulting from combined analysis of the 16S rRNA and rpoB datasets showed that the K. oxytoca isolates were monophyletic and separated into two clades; these clades included strains with either the bla(OXY-1) gene or the bla(OXY-2) gene. This result was supported with high bootstrap values of 97 and 99%, respectively. Moreover, the two groups of strains displayed distinct ERIC-1R profiles, with bands characteristic of each profile. Thus, the chromosomal bla(OXY) gene sequence is able to delineate not only two groups of beta-lactamases in K. oxytoca, but also two clades in the K. oxytoca taxon, in a manner similar to the sequence of housekeeping genes. These results suggest that K. oxytoca should be divided into two genetic groups, group OXY-1 represented by K. oxytoca strain SL781 (=CIP 104963) and group OXY-2 by K. oxytoca strain SL91l (= CIP 106098).

Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937.

Phylogenetic analyses based on partial 18S rDNA sequences of polyonchoinean monogeneans were conducted in order to investigate the relationships between selected families and subfamilies of the Dactylogyrinea, mainly within the Dactylogyridae. We tested the status of the Ancyrocephalidae sensu Bychowsky & Nagibina (1978) and the Ancyrocephalinae sensu Kritsky & Boeger (1989). Within the Dactylogyrinea, the Diplectanidae and Dactylogyridae are well supported by maximum likelihood and maximum parsimony analyses, but their phylogenetic relationship with the Pseudomurraytrematidae remains unresolved. Phylogenetic relationships between the Pseudodactylogyrinae, Ancyrocephalinae, Ancylodiscoidinae and Dactylogyrinae indicate paraphyly of the Ancyrocephalidae sensu Bychowsky & Nagibina (1978). The group of species recently considered as the Dactylogyridae sensu Kritsky & Boeger (1989) comprises two sister groups. The first group includes the freshwater Ancyrocephalinae and the Ancylodiscoidinae. The second group includes the Pseudodactylogyrinae, Dactylogyrinae and the Ancyrocephalinae from the fish species Siganus doliatus and Tetraodon fluviatilis. The non-monophyly of the Ancyrocephalinae (i.e. the non-monophyly of the group of species recently considered as members of Ancyrocephalinae), previously suggested by Kritsky & Boeger (1989) using the morphological characters, indicates that classification of the Dactylogyridae needs to be revised.

Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans.

We reviewed several published and ongoing studies concerning monogenean communities. Patterns of species richness, host specificity, community structure and host--parasite coevolutionary interaction were carefully analysed, and hypotheses of evolutionary processes are proposed. The structuring of monogenean communities seems to be related to both ecological and historical constraints. The database supports an absence of intra- and interspecific competition in monogeneans. Species richness seems to be more due to host characteristics than to parasite interactions. Monogeneans seem to specialise on large hosts, leading to greater species richness on those hosts. The morphometric evolution of attachment and copulatory organs support the hypothesis of a reproductive segregation among conspecifics parasitising the same host(s). It also suggests the existence of concurrent adaptive and non-adaptive processes. The general absence of a coevolutionary pattern between host and parasites also suggests the constraints of history without dismissing the influences of ecological factors in the structuring of the communities. More generally, we strengthen the need to study the structure of communities in a phylogenetic context.