Rebounds, regresses, and recovery: A 15-year study of the coral reef community at Pila'a, Kaua'i after decades of natural and anthropogenic stress events.

Pila'a reef on the north shore of Kaua'i, Hawai'i was subjected to a major flood event in 2001 that deposited extensive sediment on the reef flat, resulting in high coral mortality. To document potential recovery, this study replicated benthic and sediment surveys conducted immediately following the event and 15 years later. Coral cores were analyzed to determine coral growth rates and density. Our results suggest that significant reduction in terrigenous sediments has led to partial ecosystem recovery based on coral species and colony increases, more balanced size frequency distributions, improved coral condition, and enhanced coral recruitment despite lack of recovery of large dead coral colonies. However, within this 15-year period, episodic storms and a bleaching event impeded the recovery process, preventing full recovery and continuously threatening the coral reef community. As climate change progresses, the intensity and frequency of these disturbances are predicted to increase.

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.

Expanding the repertoire of electron acceptors for the anaerobic oxidation of methane in carbonates in the Atlantic and Pacific Ocean.

Authigenic carbonates represent a significant microbial sink for methane, yet little is known about the microbiome responsible for the methane removal. We identify carbonate microbiomes distributed over 21 locations hosted by seven different cold seeps in the Pacific and Atlantic Oceans by carrying out a gene-based survey using 16S rRNA- and mcrA gene sequencing coupled with metagenomic analyses. Based on 16S rRNA gene amplicon analyses, these sites were dominated by bacteria affiliated to the Firmicutes, Alpha- and Gammaproteobacteria. ANME-1 and -2 archaeal clades were abundant in the carbonates yet their typical syntrophic partners, sulfate-reducing bacteria, were not significantly present. Based on mcrA amplicon analyses, the Candidatus Methanoperedens clades were also highly abundant. Our metagenome analysis indicated that methane oxidizers affiliated to the ANME-1 and -2, may be capable of performing complete methane- and potentially short-chain alkane oxidation independently using oxidized sulfur and nitrogen compounds as terminal electron acceptors. Gammaproteobacteria are hypothetically capable of utilizing oxidized nitrogen compounds and may be involved in syntrophy with methane-oxidizing archaea. Carbonate structures represent a window for a more diverse utilization of electron acceptors for anaerobic methane oxidation along the Atlantic and Pacific Margin.

Coral Skeleton δ15N as a Tracer of Historic Nutrient Loading to a Coral Reef in Maui, Hawaii.

Excess nutrient loading to nearshore environments has been linked to declining water quality and ecosystem health. Macro-algal blooms, eutrophication, and reduction in coral cover have been observed in West Maui, Hawaii, and linked to nutrient inputs from coastal submarine groundwater seeps. Here, we present a forty-year record of nitrogen isotopes (δ15N) of intra-crystalline coral skeletal organic matter in three coral cores collected at this site and evaluate the record in terms of changes in nitrogen sources. Our results show a dramatic increase in coral δ15N values after 1995, corresponding with the implementation of biological nutrient removal at the nearby Lahaina Wastewater Reclamation Facility (LWRF). High δ15N values are known to be strongly indicative of denitrification and sewage effluent, corroborating a previously suggested link between local wastewater injection and degradation of the reef environment. This record demonstrates the power of coral skeletal δ15N as a tool for evaluating nutrient dynamics within coral reef environments.

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.

Uptake and distribution of organo-iodine in deep-sea corals.

Understanding iodine concentration, transport, and bioavailability is essential in evaluating iodine's impact to the environment and its effectiveness as an environmental biogeotracer. While iodine and its radionuclides have proven to be important tracers in geologic and biologic studies, little is known about transport of this element to the deep sea and subsequent uptake in deep-sea coral habitats. Results presented here on deep-sea black coral iodine speciation and iodine isotope variability provides key information on iodine behavior in natural and anthropogenic environments, and its geochemical pathway in the Gulf of Mexico. Organo-iodine is the dominant iodine species in the black corals, demonstrating that binding of iodine to organic matter plays an important role in the transport and transfer of iodine to the deep-sea corals. The identification of growth bands captured in high-resolution scanning electron images (SEM) with synchronous peaks in iodine variability suggest that riverine delivery of terrestrial-derived organo-iodine is the most plausible explanation to account for annual periodicity in the deep-sea coral geochemistry. Whereas previous studies have suggested the presence of annual growth rings in deep-sea corals, this present study provides a mechanism to explain the formation of annual growth bands. Furthermore, deep-sea coral ages based on iodine peak counts agree well with those ages derived from radiocarbon (14C) measurements. These results hold promise for developing chronologies independent of 14C dating, which is an essential component in constraining reservoir ages and using radiocarbon as a tracer of ocean circulation. Furthermore, the presence of enriched 129I/127I ratios during the most recent period of skeleton growth is linked to nuclear weapons testing during the 1960s. The sensitivity of the coral skeleton to record changes in surface water 129I composition provides further evidence that iodine composition and isotope variability captured in proteinaceous deep-sea corals is a promising geochronometer as well as an emerging tracer for continental material flux.

Reconstructing surface ocean circulation with 129I time series records from corals.

The long-lived radionuclide 129I (half-life: 15.7 × 106 yr) is well-known as a useful environmental tracer. At present, the global 129I in surface water is about 1-2 orders of magnitude higher than pre-1960 levels. Since the 1990s, anthropogenic 129I produced from industrial nuclear fuels reprocessing plants has been the primary source of 129I in marine surface waters of the Atlantic and around the globe. Here we present four coral 129I time series records from: 1) Con Dao and 2) Xisha Islands, the South China Sea, 3) Rabaul, Papua New Guinea and 4) Guam. The Con Dao coral 129I record features a sudden increase in 129I in 1959. The Xisha coral shows similar peak values for 129I as the Con Dao coral, punctuated by distinct low values, likely due to the upwelling in the central South China Sea. The Rabaul coral features much more gradual 129I increases in the 1970s, similar to a published record from the Solomon Islands. The Guam coral 129I record contains the largest measured values for any site, with two large peaks, in 1955 and 1959. Nuclear weapons testing was the primary 129I source in the Western Pacific in the latter part of the 20th Century, notably from testing in the Marshall Islands. The Guam 1955 peak and Con Dao 1959 increases are likely from the 1954 Castle Bravo test, and the Operation Hardtack I test is the most likely source of the 1959 peak observed at Guam. Radiogenic iodine found in coral was carried primarily through surface ocean currents. The coral 129I time series data provide a broad picture of the surface distribution and depth penetration of 129I in the Pacific Ocean over the past 60 years.

Coral Ba/Ca records of sediment input to the fringing reef of the southshore of Moloka'i, Hawai'i over the last several decades.

The fringing reef of southern Moloka'i is perceived to be in decline because of land-based pollution. In the absence of historical records of sediment pollution, ratios of coral Ba/Ca were used to test the hypothesis that sedimentation has increased over time. Baseline Ba/Ca ratios co-vary with the abundance of red, terrigenous sediment visible in recent imagery. The highest values at One Ali'i are near one of the muddiest parts of the reef. This co-varies with the lowest growth rate of all the sites, perhaps because the upstream Kawela watershed was historically leveed all the way to the nearshore, providing a fast-path for sediment delivery. Sites adjacent to small, steep watersheds have ∼decadal periodicities whereas sites adjacent to mangrove forests have shorter-period fluctuations that correspond to the periodicity of sediment transport in the nearshore, rather than the watershed. All four sites show a statistically significant upward trend in Ba/Ca.

Century-scale records of land-based activities recorded in Mesoamerican coral cores.

The Mesoamerican Reef, the second-largest barrier reef in the world, is located in the western Caribbean Sea off the coasts of Mexico, Belize, Guatemala, and Honduras. Particularly in the south, the surrounding watersheds are steep and the climate is extremely wet. With development and agricultural expansion, the potential for negative impacts to the reef from land-based runoff becomes high. We constructed annually resolved century-scale records of metal/calcium ratios in coral skeletons collected from four sites experiencing a gradient of land-based runoff. Our proxy data indicate that runoff onto the reef has increased relatively steadily over time at all sites, consistent with land use trends from historical records. Sediment supply to the reef is greater in the south, and these more exposed reefs will probably benefit most immediately from management that targets runoff reduction. However, because runoff at all sites is steadily increasing, even distal sites will benefit from watershed management.