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  • 1
    Publication Date: 2022-05-25
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Moore, M. J., Rowles, T. K., Fauquier, D. A., Baker, J. D., Biedron, I., Durban, J. W., Hamilton, P. K., Henry, A. G., Knowlton, A. R., McLellan, W. A., Miller, C. A., Pace, R. M.,3rd, Pettis, H. M., Raverty, S., Rolland, R. M., Schick, R. S., Sharp, S. M., Smith, C. R., Thomas, L., der Hoop, J. M. V., & Ziccardi, M. H. REVIEW: Assessing North Atlantic right whale health: threats, and development of tools critical for conservation of the species. Diseases of Aquatic Organisms, 143, (2021): 205-226, https://doi.org/10.3354/dao03578.
    Description: Whaling decimated North Atlantic right whales (Eubalaena glacialis - NARW) since the 11th century and southern right whales (E. australis - SRW) since the 19th century. Today, NARWs are critically endangered and decreasing, whereas SRWs are recovering. We review NARW health assessment literature, NARW Consortium databases, and efforts and limitations to monitor individual and species health, survival, and fecundity. Photographs are used to track individual movement and external signs of health such as evidence of vessel and entanglement trauma. Post mortem examinations establish cause of death and determine organ pathology. Photogrammetry is used to assess growth rates and body condition. Samples of blow, skin, blubber, baleen and feces quantify hormones that provide information on stress, reproduction, and nutrition, identify microbiome changes, and assess evidence of infection. We also discuss models of the population consequences of multiple stressors, including the connection between human activities (e.g., entanglement) and health. Lethal and sublethal vessel and entanglement trauma have been identified as major threats to the species. There is a clear and immediate need for expanding trauma reduction measures. Beyond these major concerns, further study is needed to evaluate the impact of other stressors, such as pathogens, microbiome changes, and algal and industrial toxins, on NARW reproductive success and health. Current and new health assessment tools should be developed and used to monitor the effectiveness of management measures, and will help determine whether they are sufficient for a substantive species recovery.
    Description: We thank the participants of the North Atlantic Right Whale Health Assessment workshop, June 24-26, 2019, Silver Spring MD, USA, for their contributions. NA14OAR4320158 funded the drafting of this manuscript. We sincerely thank three anonymous reviewers for their constructive comments. The scientific results and conclusions, as well as any views or opinions expressed herein, are those of the authors and do not necessarily reflect the views of NOAA.
    Keywords: Right Whale ; Health ; Trauma ; Reproduction ; Stressor ; Cumulative Effects
    Repository Name: Woods Hole Open Access Server
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  • 2
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Christiansen, F., Dawson, S. M., Durban, J. W., Fearnbach, H., Miller, C. A., Bejder, L., Uhart, M., Sironi, M., Corkeron, P., Rayment, W., Leunissen, E., Haria, E., Ward, R., Warick, H. A., Kerr, I., Lynn, M. S., Pettis, H. M., & Moore, M. J. Population comparison of right whale body condition reveals poor state of the North Atlantic right whale. Marine Ecology Progress Series, 640, (2020): 1-16, doi:10.3354/meps13299.
    Description: The North Atlantic right whale Eubalaena glacialis (NARW), currently numbering 〈410 individuals, is on a trajectory to extinction. Although direct mortality from ship strikes and fishing gear entanglements remain the major threats to the population, reproductive failure, resulting from poor body condition and sublethal chronic entanglement stress, is believed to play a crucial role in the population decline. Using photogrammetry from unmanned aerial vehicles, we conducted the largest population assessment of right whale body condition to date, to determine if the condition of NARWs was poorer than 3 seemingly healthy (i.e. growing) populations of southern right whales E. australis (SRWs) in Argentina, Australia and New Zealand. We found that NARW juveniles, adults and lactating females all had lower body condition scores compared to the SRW populations. While some of the difference could be the result of genetic isolation and adaptations to local environmental conditions, the magnitude suggests that NARWs are in poor condition, which could be suppressing their growth, survival, age of sexual maturation and calving rates. NARW calves were found to be in good condition. Their body length, however, was strongly determined by the body condition of their mothers, suggesting that the poor condition of lactating NARW females may cause a reduction in calf growth rates. This could potentially lead to a reduction in calf survival or an increase in female calving intervals. Hence, the poor body condition of individuals within the NARW population is of major concern for its future viability.
    Description: North Atlantic: NOAA NA14OAR4320158; Australia: US Office of Naval Research Marine Mammals Program (Award No. N00014-17-1-3018), the World Wildlife Fund for Nature Australia and a Murdoch University School of Veterinary and Life Sciences Small Grant Award; New Zealand: New Zealand Antarctic Research institute (NZARI 2016-1-4), Otago University and NZ Whale and Dolphin Trust; Argentina: National Geographic Society (Grant number: NGS-379R-18).
    Keywords: Baleen whale ; Bioenergetics ; Eubalaena ; Morphometrics ; Photogrammetry ; Unmanned aerial vehicles
    Repository Name: Woods Hole Open Access Server
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  • 3
    Publication Date: 2022-10-07
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Stewart, J., Durban, J., Europe, H., Fearnbach, H., Hamilton, P., Knowlton, A., Lynn, M., Miller, C., Perryman, W., Tao, B., & Moore, M. Larger females have more calves: influence of maternal body length on fecundity in North Atlantic right whales. Marine Ecology Progress Series, 689, (2022): 179–189, https://doi.org/10.3354/meps14040.
    Description: North Atlantic right whales (NARW) are critically endangered and have been declining in abundance since 2011. In the past decade, human-caused mortalities from vessel strikes and entanglements have been increasing, while birth rates in the population are at a 40 yr low. In addition to declining abundance, recent studies have shown that NARW length-at-age is decreasing due to the energetic impacts of sub-lethal entanglements, and that the body condition of the population is poorer than closely related southern right whales. We examined whether shorter body lengths are associated with reduced fecundity in female NARW. We compared age-corrected, modeled metrics of body length with 3 metrics of fecundity: age at first reproduction, average inter-birth interval, and the number of calves produced per potential reproductive year. We found that body length is significantly related to birth interval and calves produced per reproductive year, but not age at first reproduction. Larger whales had shorter inter-birth intervals and produced more calves per potential reproductive year. Larger whales also had higher lifetime calf production, but this was a result of larger whales having longer potential reproductive spans, as body lengths have generally been declining over the past 40 yr. Declining body sizes are a potential contributor to low birth rates over the past decade. Efforts to reduce entanglements and vessel strikes could help maintain population viability by increasing fecundity and improving resiliency of the population to other anthropogenic and climate impacts.
    Description: Funding to the New England Aquarium for curation of the photo-identification catalog is provided by NOAA Contract 1305M2- 18-P-NFFM-0108.
    Keywords: Photogrammetry ; Cetacean ; Reproduction ; Anthropogenic impacts
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  • 4
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Millette, N. C., da Costa, M., Mora, J. W., & Gast, R. J. Temporal and spatial variability of phytoplankton and mixotrophs in a temperate estuary. Marine Ecology Progress Series, 677, (2021): 17–3,. https://doi.org/10.3354/meps13850.
    Description: A significant proportion of phototrophic species are known to be mixotrophs: cells that obtain nutrients through a combination of photosynthesis and prey ingestion. Current methods to estimate mixotroph abundance in situ are known to be limited in their ability to help identify conditions that favor mixotrophs over strict autotrophs. For the first time, we combine microscopic analysis of phototrophic taxa with immunoprecipitated bromodeoxyuridine (BrdU)-labeled DNA amplicon sequencing to identify and quantify active and putative mixotrophs at 2 locations in a microtidal temperate estuary. We analyze these data to examine spatial and temporal variability of phytoplankton and mixotrophs. Microscopy-based phototrophic diversity and abundances reveal expected seasonal patterns for our 2 stations, with the start of growth in winter and highest abundances in summer. Diatoms tend to dominate at the site with less stratification, while dinoflagellates and euglenids are usually more prominent at the stratified station. The BrdU-based mixotroph identifications are translated to the microscopy identification and abundances to estimate the proportion of mixotrophs (cells 〉10 µm in size) at both sites. The average proportion of potential mixotrophs is higher at the station with higher stratification (51%) compared to the station with lower stratification (30%), and potential mixotrophs tend to be higher in summer, although we did not conduct BrdU experiments in any of the other seasons. Combining the identification of active mixotrophs through the uptake of BrdU-labeled bacteria with robust abundance measurements can expand our understanding of mixotrophs across systems.
    Description: N.C.M. was funded by a Woods Hole Sea Grant Postdoctoral Fellowship (award number NA14OAR4170074), and M.dC. was funded by a WHOI Summer Student Fellowship. This is VIMS contribution number 4057.
    Keywords: Phytoplankton ; Mixotrophs ; Estuaries ; Chl a
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  • 5
    Publication Date: 2022-07-28
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lonati, G., Zitterbart, D. P., Miller, C. A., Corkeron, P. J., Murphy, C. T., & Moore, M. J. Investigating the thermal physiology of critically endangered North Atlantic right whales Eubalaena glacialis via aerial infrared thermography. Endangered Species Research, 48, (2022): 139–154, https://doi.org/10.3354/esr01193.
    Description: The Critically Endangered status of North Atlantic right whales Eubalaena glacialis (NARWs) warrants the development of new, less invasive technology to monitor the health of individuals. Combined with advancements in remotely piloted aircraft systems (RPAS, commonly ‘drones’), infrared thermography (IRT) is being increasingly used to detect and count marine mammals and study their physiology. We conducted RPAS-based IRT over NARWs in Cape Cod Bay, MA, USA, in 2017 and 2018. Observations demonstrated 3 particularly useful applications of RPAS-based IRT to study large whales: (1) exploring patterns of cranial heat loss and providing insight into the physiological mechanisms that produce these patterns; (2) tracking subsurface individuals in real-time (depending on the thermal stratification of the water column) using cold surface water anomalies resulting from fluke upstrokes; and (3) detecting natural changes in superficial blood circulation or diagnosing pathology based on heat anomalies on post-cranial body surfaces. These qualitative applications present a new, important opportunity to study, monitor, and conserve large whales, particularly rare and at-risk species such as NARWs. Despite the challenges of using this technology in aquatic environments, the applications of RPAS-based IRT for monitoring the health and behavior of endangered marine mammals, including the collection of quantitative data on thermal physiology, will continue to diversify.
    Description: All activities were conducted under NOAA permit 18355-01 and were approved by Woods Hole Oceanographic Institution’s Institutional Animal Care and Use Committee (IACUC). The RPAS pilot-in-command was certified through the United States Federal Aviation Admin-istration. We thank Amy Knowlton (Anderson Cabot Center for Ocean Life at the New England Aquarium) for photo-identifying individual North Atlantic right whales and Rocky Geyer (Woods Hole Oceanographic Institution) for providing and interpreting water temperature data relatedto the observations of thermal flukeprints (courtesy of the Massachusetts Water Resources Authority). We also appreciate constructive conversations with Iain Kerr (Ocean Alliance), Chris Zadra (Ocean Alliance), and Joy Reidenberg (Icahn School of Medicine at Mount Sinai). Funding was provided by a Woods Hole Oceanographic Research Opportunity grant, the North Pond Foundation, and NMFS NA14OAR4320158.
    Keywords: Cetaceans ; Drone ; Health ; Marine mammals ; Remote sensing ; Temperature ; UAVs
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  • 6
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Caiger, P. E., Dean, M. J., DeAngelis, A. I., Hatch, L. T., Rice, A. N., Stanley, J. A., Tholke, C., Zemeckis, D. R., & Van Parijs, S. M. A decade of monitoring Atlantic cod Gadus morhua spawning aggregations in Massachusetts Bay using passive acoustics. Marine Ecology Progress Series, 635, (2020): 89-103, doi:10.3354/meps13219.
    Description: Atlantic cod Gadus morhua populations in the northeast USA have failed to recover since major declines in the 1970s and 1990s. To rebuild these stocks, managers need reliable information on spawning dynamics in order to design and implement control measures; discovering cost-effective and non-invasive monitoring techniques is also favorable. Atlantic cod form dense, site-fidelic spawning aggregations during which they vocalize, permitting acoustic detection of their presence at such times. The objective of this study was to detect spawning activity of Atlantic cod using multiple fixed-station passive acoustic recorders to sample across Massachusetts Bay during the winter spawning period. A generalized linear modeling approach was used to investigate spatio-temporal trends of cod vocalizing over 10 consecutive winter spawning seasons (2007-2016), the longest such timeline of any passive acoustic monitoring of a fish species. The vocal activity of Atlantic cod was associated with diel, lunar, and seasonal cycles, with a higher probability of occurrence at night, during the full moon, and near the end of November. Following 2009 and 2010, there was a general decline in acoustic activity. Furthermore, the northwest corner of Stellwagen Bank was identified as an important spawning location. This project demonstrated the utility of passive acoustic monitoring in determining the presence of an acoustically active fish species, and provides valuable data for informing the management of this commercially, culturally, and ecologically important species.
    Description: Thanks to Eli Bonnell, Genevieve Davis, Julianne Bonell, Samara Haver, and Eric Matzen for assistance in MARU deployments, Dana Gerlach and Heather Heenehan for help in passive acoustic data analysis, and the NEFSC passive acoustics group for useful discussions. Funding for 2007−2012 passive acoustic surveys was provided by Excelerate Energy and Neptune LNG to Cornell University. Fieldwork for 2013−2015 was funded through the 2013−2014 NOAA Saltonstall-Kennedy grant program (Award No. NA14NMF4270027), and jointly funded by The Nature Conservancy, Massachusetts Division of Marine Fisheries, and the Cabot Family Charitable Foundation. Funding for 2016 SoundTrap data was provided by NOAA’s Ocean Acoustics Program (4 Sanctuaries Project).
    Keywords: Atlantic cod ; Passive acoustic monitoring ; Gadus morhua ; Massachusetts Bay ; Spawning aggregations ; Fisheries management
    Repository Name: Woods Hole Open Access Server
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  • 7
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Becker, C. C., Weber, L., Suca, J. J., Llopiz, J. K., Mooney, T. A., & Apprill, A. Microbial and nutrient dynamics in mangrove, reef, and seagrass waters over tidal and diurnal time scales. Aquatic Microbial Ecology, 85, (2020): 101-119, https://doi.org/10.3354/ame01944.
    Description: In coral reefs and adjacent seagrass meadow and mangrove environments, short temporal scales (i.e. tidal, diurnal) may have important influences on ecosystem processes and community structure, but these scales are rarely investigated. This study examines how tidal and diurnal forcings influence pelagic microorganisms and nutrient dynamics in 3 important and adjacent coastal biomes: mangroves, coral reefs, and seagrass meadows. We sampled for microbial (Bacteria and Archaea) community composition, cell abundances and environmental parameters at 9 coastal sites on St. John, US Virgin Islands that spanned 4 km in distance (4 coral reefs, 2 seagrass meadows and 3 mangrove locations within 2 larger bays). Eight samplings occurred over a 48 h period, capturing day and night microbial dynamics over 2 tidal cycles. The seagrass and reef biomes exhibited relatively consistent environmental conditions and microbial community structure but were dominated by shifts in picocyanobacterial abundances that were most likely attributed to diel dynamics. In contrast, mangrove ecosystems exhibited substantial daily shifts in environmental parameters, heterotrophic cell abundances and microbial community structure that were consistent with the tidal cycle. Differential abundance analysis of mangrove-associated microorganisms revealed enrichment of pelagic oligotrophic taxa during high tide and enrichment of putative sediment-associated microbes during low tide. Our study underpins the importance of tidal and diurnal time scales in structuring coastal microbial and nutrient dynamics, with diel and tidal cycles contributing to a highly dynamic microbial environment in mangroves, and time of day likely contributing to microbial dynamics in seagrass and reef biomes.
    Description: This research was supported by NSF awards OCE-1536782 to T.A.M., J.K.L., and A.A. and OCE-1736288 to A.A., NOAA Cooperative Institutes award NA19O AR 4320074 to A.A. and E. Kujawinski and the Andrew W. Mellon Foundation Endowed Fund for Innovative Research to A.A.
    Keywords: Tide ; Picoplankton ; Mangrove ; Coral reef ; Seagrass ; Time series ; 16S rRNA gene
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  • 8
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Leslie, M. S., Perkins-Taylor, C. M., Durban, J. W., Moore, M. J., Miller, C. A., Chanarat, P., Bahamonde, P., Chiang, G., & Apprill, A. Body size data collected non-invasively from drone images indicate a morphologically distinct Chilean blue whale (Blaenoptera musculus) taxon. Endangered Species Research, 43, (2020): 291-304, https://doi.org/10.3354/esr01066.
    Description: The blue whale Balaenoptera musculus (Linnaeus, 1758) was the target of intense commercial whaling in the 20th century, and current populations remain drastically below pre-whaling abundances. Reducing uncertainty in subspecific taxonomy would enable targeted conservation strategies for the recovery of unique intraspecific diversity. Currently, there are 2 named blue whale subspecies in the temperate to polar Southern Hemisphere: the Antarctic blue whale B. m. intermedia and the pygmy blue whale B. m. brevicauda. These subspecies have distinct morphologies, genetics, and acoustics. In 2019, the Society for Marine Mammalogy’s Committee on Taxonomy agreed that evidence supports a third (and presently unnamed) subspecies of Southern Hemisphere blue whale subspecies, the Chilean blue whale. Whaling data indicate that the Chilean blue whale is intermediate in body length between pygmy and Antarctic blue whales. We collected body size data from blue whales in the Gulfo Corcovado, Chile, during the austral summers of 2015 and 2017 using aerial photogrammetry from a remotely controlled drone to test the hypothesis that the Chilean blue whale is morphologically distinct from other Southern Hemisphere blue whale subspecies. We found the Chilean whale to be morphologically intermediate in both overall body length and relative tail length, thereby joining other diverse data in supporting the Chilean blue whale as a unique subspecific taxon. Additional photogrammetry studies of Antarctic, pygmy, and Chilean blue whales will help examine unique morphological variation within this species of conservation concern. To our knowledge, this is the first non-invasive small drone study to test a hypothesis for systematic biology.
    Description: We are thankful to Foundation MERI (Melimoyu Ecosystem Research Institute) for logistical and funding support. Cruise support in 2017 was provided by the Dalio Foundation (now ‘OceanX’).
    Keywords: Aerial photogrammetry ; Taxonomy ; Subspecies ; Whaling ; Systematics ; Unoccupied aerial systems ; UAS
    Repository Name: Woods Hole Open Access Server
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  • 9
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Jackson, J. A., Kennedy, A., Moore, M., Andriolo, A., Bamford, C. C. G., Calderan, S., Cheeseman, T., Gittins, G., Groch, K., Kelly, N., Leaper, R., Leslie, M. S., Lurcock, S., Miller, B. S., Richardson, J., Rowntree, V., Smith, P., Stepien, E., Stowasser, G., Trathan, P., Vermeulen, E., Zerbini, A. N., & Carroll, E. L. Have whales returned to a historical hotspot of industrial whaling? the pattern of southern right whale Eubalaena australis recovery at South Georgia. Endangered Species Research, 43, (2020): 323-339, https://doi.org/10.3354/esr01072.
    Description: Around 176500 whales were killed in the sub-Antarctic waters off South Georgia (South Atlantic) between 1904 and 1965. In recent decades, whales have once again become summer visitors, with the southern right whale (SRW) the most commonly reported species until 2011. Here, we assess the distribution, temporal pattern, health status and likely prey of SRWs in these waters, combining observations from a summertime vessel-based expedition to South Georgia, stable isotope data collected from SRWs and putative prey and sightings reports collated by the South Georgia Museum. The expedition used directional acoustics and visual surveys to localise whales and collected skin biopsies and photo-IDs. During 76 h of visual observation effort over 19 expedition days, SRWs were encountered 15 times (~31 individuals). Photo-IDs, combined with publicly contributed images from commercial vessels, were reconciled and quality-controlled to form a catalogue of 6 fully (i.e. both sides) identified SRWs and 26 SRWs identified by either left or right sides. No photo-ID matches were found with lower-latitude calving grounds, but 3 whales had gull lesions supporting a direct link with Península Valdés, Argentina. The isotopic position of SRWs in the South Georgia food web suggests feeding on a combination of copepod and krill species. Opportunistic reports of SRW sightings and associated group sizes remain steady over time, while humpback whales provide a strong contrast, with increased sighting rates and group sizes seen since 2013. These data suggest a plateau in SRWs and an increasing humpback whale presence in South Georgia waters following the cessation of whaling.
    Description: This work was supported by funding from an EU BEST 2.0 Medium Grant 1594, with additional support provided by a DARWIN PLUS award DPLUS057and additional funding from the World Wildlife Fund. E.L.C. was partially supported by a Rutherford Discovery Fellowship from the Royal Society of New Zealand.
    Keywords: Eubalaena australis ; Whale ; Whaling ; Antarctic ; Recovery ; Habitat use
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  • 10
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Apprill, A., Holm, H., Santoro, A. E., Becker, C., Neave, M., Hughen, K., Richards Dona, A., Aeby, G., Work, T., Weber, L., & McNally, S. Microbial ecology of coral-dominated reefs in the Federated States of Micronesia. Aquatic Microbial Ecology, 86, (2021): 115–136, https://doi.org/10.3354/ame01961.
    Description: Microorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km2. On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (〉85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features.
    Description: Samples were collected under Federated States of Micronesia collection permits FM12-11-03S and FM12-11-05S. This project was supported by funding to A.A.: Woods Hole Oceanographic Institution Access to the Sea, Dalio Family Foundation, Andrew W. Mellon Foundation Endowed Fund for Innovative Research, and National Science Foundation awards OCE- 1233612 and OCE-1736288. A.E.S. was supported by startup funds from the University of Maryland Center for Environmental Sciences. K.H. obtained funding from WHOI Access to the Sea and the Dalio Explore Foundation that supported this cruise.
    Keywords: Coral reef ; Microbiology ; Micronesia ; Oligotrophic ; Cyanobacteria ; SSU rRNA gene
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