Expanding our view of the cold-water coral niche and accounting of the ecosystem services of the reef habitat.

Coral reefs are iconic ecosystems that support diverse, productive communities in both shallow and deep waters. However, our incomplete knowledge of cold-water coral (CWC) niche space limits our understanding of their distribution and precludes a complete accounting of the ecosystem services they provide. Here, we present the results of recent surveys of the CWC mound province on the Blake Plateau off the U.S. east coast, an area of intense human activity including fisheries and naval operations, and potentially energy and mineral extraction. At one site, CWC mounds are arranged in lines that total over 150 km in length, making this one of the largest reef complexes discovered in the deep ocean. This site experiences rapid and extreme shifts in temperature between 4.3 and 10.7 °C, and currents approaching 1 m s-1. Carbon is transported to depth by mesopelagic micronekton and nutrient cycling on the reef results in some of the highest nitrate concentrations recorded in the region. Predictive models reveal expanded areas of highly suitable habitat that currently remain unexplored. Multidisciplinary exploration of this new site has expanded understanding of the cold-water coral niche, improved our accounting of the ecosystem services of the reef habitat, and emphasizes the importance of properly managing these systems.

Genetic diversity and connectivity of chemosynthetic cold seep mussels from the U.S. Atlantic margin.

BACKGROUND: Deep-sea mussels in the subfamily Bathymodiolinae have unique adaptations to colonize hydrothermal-vent and cold-seep environments throughout the world ocean. These invertebrates function as important ecosystem engineers, creating heterogeneous habitat and promoting biodiversity in the deep sea. Despite their ecological significance, efforts to assess the diversity and connectivity of this group are extremely limited. Here, we present the first genomic-scale diversity assessments of the recently discovered bathymodioline cold-seep communities along the U.S. Atlantic margin, dominated by Gigantidas childressi and Bathymodiolus heckerae. RESULTS: A Restriction-site Associated DNA Sequencing (RADSeq) approach was used on 177 bathymodiolines to examine genetic diversity and population structure within and between seep sites. Assessments of genetic differentiation using single-nucleotide polymorphism (SNP) data revealed high gene flow among sites, with the shallower and more northern sites serving as source populations for deeper occurring G. childressi. No evidence was found for genetic diversification across depth in G. childressi, likely due to their high dispersal capabilities. Kinship analyses indicated a high degree of relatedness among individuals, and at least 10-20% of local recruits within a particular site. We also discovered candidate adaptive loci in G. childressi and B. heckerae that suggest differences in developmental processes and depth-related and metabolic adaptations to chemosynthetic environments. CONCLUSIONS: These results highlight putative source communities for an important ecosystem engineer in the deep sea that may be considered in future conservation efforts. Our results also provide clues into species-specific adaptations that enable survival and potential speciation within chemosynthetic ecosystems.

New geochemical tools for investigating resource and energy functions at deep-sea cold seeps using amino acid δ15 N in chemosymbiotic mussels (Bathymodiolus childressi).

In order to reconstruct the ecosystem structure of chemosynthetic environments in the fossil record, geochemical proxies must be developed. Here, we present a suite of novel compound-specific isotope parameters for tracing chemosynthetic production with a focus on understanding nitrogen dynamics in deep-sea cold seep environments. We examined the chemosymbiotic bivalve Bathymodiolus childressi from three geographically distinct seep sites on the NE Atlantic Margin and compared isotope data to non-chemosynthetic littoral mussels to test whether water depth, seep activity, and/or mussel bed size are linked to differences in chemosynthetic production. The bulk isotope analysis of carbon (δ13 C) and nitrogen (δ15 N), and δ15 N values of individual amino acids (δ15 NAA ) in both gill and muscle tissues, as well as δ15 NAA- derived parameters including trophic level (TL), baseline δ15 N value (δ15 NPhe ), and a microbial resynthesis index (ΣV), were used to investigate specific geochemical signatures of chemosynthesis. Our results show that δ15 NAA values provide a number of new proxies for relative reliance on chemosynthesis, including TL, ∑V, and both δ15 N values and molar percentages (Gly/Glu mol% index) of specific AA. Together, these parameters suggested that relative chemoautotrophy is linked to both degree of venting from seeps and mussel bed size. Finally, we tested a Bayesian mixing model using diagnostic AA δ15 N values, showing that percent contribution of chemoautotrophic versus heterotrophic production to seep mussel nutrition can be directly estimated from δ15 NAA values. Our results demonstrate that δ15 NAA analysis can provide a new set of geochemical tools to better understand mixotrophic ecosystem function and energetics, and suggest extension to the study of ancient chemosynthetic environments in the fossil record.

Distribution of deep-water scleractinian and stylasterid corals across abiotic environmental gradients on three seamounts in the Anegada Passage.

In the Caribbean Basin the distribution and diversity patterns of deep-sea scleractinian corals and stylasterid hydrocorals are poorly known compared to their shallow-water relatives. In this study, we examined species distribution and community assembly patterns of scleractinian and stylasterid corals on three high-profile seamounts within the Anegada Passage, a deep-water throughway linking the Caribbean Sea and western North Atlantic. Using remotely operated vehicle surveys conducted on the E/V Nautilus by the ROV Hercules in 2014, we characterized coral assemblages and seawater environmental variables between 162 and 2,157 m on Dog Seamount, Conrad Seamount, and Noroît Seamount. In all, 13 morphospecies of scleractinian and stylasterid corals were identified from video with stylasterids being numerically more abundant than both colonial and solitary scleractinians. Cosmopolitan framework-forming species including Madrepora oculata and Solenosmilia variabilis were present but occurred in patchy distributions among the three seamounts. Framework-forming species occurred at or above the depth of the aragonite saturation horizon with stylasterid hydrocorals being the only coral taxon observed below Ωarag values of 1. Coral assemblage variation was found to be strongly associated with depth and aragonite saturation state, while other environmental variables exerted less influence. This study enhances our understanding of the factors that regulate scleractinian and stylasterid coral distribution in an underreported marginal sea and establishes a baseline for monitoring future environmental changes due to ocean acidification and deoxygenation in the tropical western Atlantic.

Molecular characterization of Bathymodiolus mussels and gill symbionts associated with chemosynthetic habitats from the U.S. Atlantic margin.

Mussels of the genus Bathymodiolus are among the most widespread colonizers of hydrothermal vent and cold seep environments, sustained by endosymbiosis with chemosynthetic bacteria. Presumed species of Bathymodiolus are abundant at newly discovered cold seeps on the Mid-Atlantic continental slope, however morphological taxonomy is challenging, and their phylogenetic affinities remain unestablished. Here we used mitochondrial sequence to classify species found at three seep sites (Baltimore Canyon seep (BCS; ~400m); Norfolk Canyon seep (NCS; ~1520m); and Chincoteague Island seep (CTS; ~1000m)). Mitochondrial COI (N = 162) and ND4 (N = 39) data suggest that Bathymodiolus childressi predominates at these sites, although single B. mauritanicus and B. heckerae individuals were detected. As previous work had suggested that methanotrophic and thiotrophic interactions can both occur at a site, and within an individual mussel, we investigated the symbiont communities in gill tissues of a subset of mussels from BCS and NCS. We constructed metabarcode libraries with four different primer sets spanning the 16S gene. A methanotrophic phylotype dominated all gill microbial samples from BCS, but sulfur-oxidizing Campylobacterota were represented by a notable minority of sequences from NCS. The methanotroph phylotype shared a clade with globally distributed Bathymodiolus spp. symbionts from methane seeps and hydrothermal vents. Two distinct Campylobacterota phylotypes were prevalent in NCS samples, one of which shares a clade with Campylobacterota associated with B. childressi from the Gulf of Mexico and the other with Campylobacterota associated with other deep-sea fauna. Variation in chemosynthetic symbiont communities among sites and individuals has important ecological and geochemical implications and suggests shifting reliance on methanotrophy. Continued characterization of symbionts from cold seeps will provide a greater understanding of the ecology of these unique environments as well and their geochemical footprint in elemental cycling and energy flux.

The influence of different deep-sea coral habitats on sediment macrofaunal community structure and function.

Deep-sea corals can create a highly complex, three-dimensional structure that facilitates sediment accumulation and influences adjacent sediment environments through altered hydrodynamic regimes. Infaunal communities adjacent to different coral types, including reef-building scleractinian corals and individual colonies of octocorals, are known to exhibit higher macrofaunal densities and distinct community structure when compared to non-coral soft-sediment communities. However, the coral types have different morphologies, which may modify the adjacent sediment communities in discrete ways. Here we address: (1) how infaunal communities and their associated sediment geochemistry compare among deep-sea coral types (Lophelia pertusa, Madrepora oculata, and octocorals) and (2) do infaunal communities adjacent to coral habitats exhibit typical regional and depth-related patterns observed in the Gulf of Mexico (GOM). Sediment push cores were collected to assess diversity, composition, numerical abundance, and functional traits of macrofauna (>300 µm) across 450 kilometers in the GOM at depths ranging from 263-1,095 m. Macrofaunal density was highest in L. pertusa habitats, but similar between M. oculata and octocorals habitats. Density overall exhibited a unimodal relationship with depth, with maximum densities between 600 and 800 m. Diversity and evenness were highest in octocoral habitats; however, there was no relationship between diversity and depth. Infaunal assemblages and functional traits differed among coral habitats, with L. pertusa habitats the most distinct from both M. oculata and octocorals. These patterns could relate to differences in sediment geochemistry as L. pertusa habitats contained high organic carbon content but low proportions of mud compared to both M. oculata and octocoral habitats. Distance-based linear modeling revealed depth, mud content, and organic carbon as the primary factors in driving coral infaunal community structure, while geographic location (longitude) was the primary factor in functional trait composition, highlighting both the location and ecological differences of L. pertusa habitats from other coral habitats. Enhanced habitat structural complexity associated with L. pertusa and differences in localized hydrodynamic flow may contribute to the dissimilarities in the communities found among the coral types. Our results suggest a decoupling for infaunal coral communities from the typical depth-related density and diversity patterns present throughout soft-sediment habitats in the GOM, highlighting the importance of deep-sea corals in structuring unique communities in the nearby benthos.

Ectoparasitism on deep-sea fishes in the western North Atlantic: In situ observations from ROV surveys.

A complete understanding of how parasites influence marine ecosystem functioning requires characterizing a broad range of parasite-host interactions while determining the effects of parasitism in a variety of habitats. In deep-sea fishes, the prevalence of parasitism remains poorly understood. Knowledge of ectoparasitism, in particular, is limited because collection methods often cause dislodgment of ectoparasites from their hosts. High-definition video collected during 43 remotely operated vehicle surveys (2013-2014) provided the opportunity to examine ectoparasitism on fishes across habitats (open slope, canyon, seamount, cold seep) and depths (494-4689 m) off the northeastern U.S., while providing high-resolution images and valuable observations of fish behavior. Only 9% (n = 125 individuals) of all observed fishes (25 species) were confirmed with ectoparasites, but higher percentages (∼33%) were observed for some of the most abundant fish species (e.g., Antimora rostrata). Ectoparasites included two copepod families (Lernaeopodidae, Sphyriidae) that infected four host species, two isopod families (Cymothoidae, Aegidae) that infected three host species, and one isopod family (Gnathiidae) that infected 19 host species. Hyperparasitism was also observed. As host diversity declined with depth, ectoparasite diversity declined; only gnathiids were observed at depths down to 3260 m. Thus, gnathiids appear to be the most successful group to infect a diversity of fishes across a broad depth range in the deep sea. For three dominant fishes (A. rostrata, Nezumia bairdii, Synaphobranchus spp.), the abundance and intensity of ectoparasitism peaked in different depths and habitats depending on the host species examined. Notably, gnathiid infections were most intense on A. rostrata, particularly in submarine canyons, suggesting that these habitats may increase ectoparasite infections. Although ectoparasitism is often overlooked in deep-sea benthic communities, our results demonstrate that it occurs widely across a variety of habitats, depths, and locations and is a significant component of deep-sea biodiversity.

Exploration of the Canyon-Incised Continental Margin of the Northeastern United States Reveals Dynamic Habitats and Diverse Communities.

The continental margin off the northeastern United States (NEUS) contains numerous, topographically complex features that increase habitat heterogeneity across the region. However, the majority of these rugged features have never been surveyed, particularly using direct observations. During summer 2013, 31 Remotely-Operated Vehicle (ROV) dives were conducted from 494 to 3271 m depth across a variety of seafloor features to document communities and to infer geological processes that produced such features. The ROV surveyed six broad-scale habitat features, consisting of shelf-breaching canyons, slope-sourced canyons, inter-canyon areas, open-slope/landslide-scar areas, hydrocarbon seeps, and Mytilus Seamount. Four previously unknown chemosynthetic communities dominated by Bathymodiolus mussels were documented. Seafloor methane hydrate was observed at two seep sites. Multivariate analyses indicated that depth and broad-scale habitat significantly influenced megafaunal coral (58 taxa), demersal fish (69 taxa), and decapod crustacean (34 taxa) assemblages. Species richness of fishes and crustaceans significantly declined with depth, while there was no relationship between coral richness and depth. Turnover in assemblage structure occurred on the middle to lower slope at the approximate boundaries of water masses found previously in the region. Coral species richness was also an important variable explaining variation in fish and crustacean assemblages. Coral diversity may serve as an indicator of habitat suitability and variation in available niche diversity for these taxonomic groups. Our surveys added 24 putative coral species and three fishes to the known regional fauna, including the black coral Telopathes magna, the octocoral Metallogorgia melanotrichos and the fishes Gaidropsarus argentatus, Guttigadus latifrons, and Lepidion guentheri. Marine litter was observed on 81% of the dives, with at least 12 coral colonies entangled in debris. While initial exploration revealed the NEUS region to be both geologically dynamic and biologically diverse, further research into the abiotic conditions and the biotic interactions that influence species abundance and distribution is needed.

Enhanced understanding of ectoparasite-host trophic linkages on coral reefs through stable isotope analysis.

Parasitism, although the most common type of ecological interaction, is usually ignored in food web models and studies of trophic connectivity. Stable isotope analysis is widely used in assessing the flow of energy in ecological communities and thus is a potentially valuable tool in understanding the cryptic trophic relationships mediated by parasites. In an effort to assess the utility of stable isotope analysis in understanding the role of parasites in complex coral-reef trophic systems, we performed stable isotope analysis on three common Caribbean reef fish hosts and two kinds of ectoparasitic isopods: temporarily parasitic gnathiids (Gnathia marleyi) and permanently parasitic cymothoids (Anilocra). To further track the transfer of fish-derived carbon (energy) from parasites to parasite consumers, gnathiids from host fish were also fed to captive Pederson shrimp (Ancylomenes pedersoni) for at least 1 month. Parasitic isopods had δ(13)C and δ(15)N values similar to their host, comparable with results from the small number of other host-parasite studies that have employed stable isotopes. Adult gnathiids were enriched in (15)N and depleted in (13)C relative to juvenile gnathiids, providing insights into the potential isotopic fractionation associated with blood-meal assimilation and subsequent metamorphosis. Gnathiid-fed Pedersen shrimp also had δ(13)C values consistent with their food source and enriched in (15)N as predicted due to trophic fractionation. These results further indicate that stable isotopes can be an effective tool in deciphering cryptic feeding relationships involving parasites and their consumers, and the role of parasites and cleaners in carbon transfer in coral-reef ecosystems specifically.

Impact of the Deepwater Horizon oil spill on a deep-water coral community in the Gulf of Mexico.

To assess the potential impact of the Deepwater Horizon oil spill on offshore ecosystems, 11 sites hosting deep-water coral communities were examined 3 to 4 mo after the well was capped. Healthy coral communities were observed at all sites >20 km from the Macondo well, including seven sites previously visited in September 2009, where the corals and communities appeared unchanged. However, at one site 11 km southwest of the Macondo well, coral colonies presented widespread signs of stress, including varying degrees of tissue loss, sclerite enlargement, excess mucous production, bleached commensal ophiuroids, and covering by brown flocculent material (floc). On the basis of these criteria the level of impact to individual colonies was ranked from 0 (least impact) to 4 (greatest impact). Of the 43 corals imaged at that site, 46% exhibited evidence of impact on more than half of the colony, whereas nearly a quarter of all of the corals showed impact to >90% of the colony. Additionally, 53% of these corals' ophiuroid associates displayed abnormal color and/or attachment posture. Analysis of hopanoid petroleum biomarkers isolated from the floc provides strong evidence that this material contained oil from the Macondo well. The presence of recently damaged and deceased corals beneath the path of a previously documented plume emanating from the Macondo well provides compelling evidence that the oil impacted deep-water ecosystems. Our findings underscore the unprecedented nature of the spill in terms of its magnitude, release at depth, and impact to deep-water ecosystems.

Food web structure in exotic and native mangroves: a Hawaii-Puerto Rico comparison.

Plant invasions can fundamentally alter detrital inputs and the structure of detritus-based food webs. We examined the detrital pathways in mangrove food webs in native (Puerto Rican) and introduced (Hawaiian) Rhizophora mangle forests using a dual isotope approach and a mixing model. Based on trophic-level fractionation of 0-1 per thousand for delta(13)C and 2-3 per thousand for delta(15)N, among the invertebrates, only nematodes, oligochaetes, and nereid polychaetes from native mangroves exhibited stable isotopes consistent with a mangrove-derived diet. Certain fauna, in particular tubificid oligochaetes, had delta(13)C values consistent with the consumption of mangrove leaves, but they were depleted in (15)N, suggesting their primary nitrogen source was low in (15)N, and was possibly N(2)-fixing bacteria. In introduced mangroves, all feeding groups appeared to rely heavily on non-mangrove sources, especially phytoplankton inputs. Mixing model results and discriminant analysis showed clear separation of introduced and native mangrove sites based on differential food source utilization within feeding groups, with stronger and more diverse use of benthic foods observed in native forests. Observed differences between native and invasive mangrove food webs may be due to Hawaiian detritivores being poorly adapted to utilizing the tannin-rich, nitrogen-poor mangrove detritus. In addition, differential utilization of mangrove detritus between native and introduced mangroves may be a consequence of forest age. We postulate that increasing mangrove forest age may promote diversification of bacterial food webs important in N and S cycling. Our results also suggest a potentially important role for sulfur bacteria in supporting the most abundant infaunal consumers, nematodes, in the most mature systems.