Oceanographic drivers of deep-sea coral species distribution and community assembly on seamounts, islands, atolls, and reefs within the Phoenix Islands Protected Area

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Auscavitch, S. R., Deere, M. C., Keller, A. G., Rotjan, R. D., Shank, T. M., & Cordes, E. E. Oceanographic drivers of deep-sea coral species distribution and community assembly on seamounts, islands, atolls, and reefs within the Phoenix Islands Protected Area. Frontiers in Marine Science, 7, (2020): 42, doi:10.3389/fmars.2020.00042.The Phoenix Islands Protected Area, in the central Pacific waters of the Republic of Kiribati, is a model for large marine protected area (MPA) development and maintenance, but baseline records of the protected biodiversity in its largest environment, the deep sea (>200 m), have not yet been determined. In general, the equatorial central Pacific lacks biogeographic perspective on deep-sea benthic communities compared to more well-studied regions of the North and South Pacific Ocean. In 2017, explorations by the NOAA ship Okeanos Explorer and R/V Falkor were among the first to document the diversity and distribution of deep-water benthic megafauna on numerous seamounts, islands, shallow coral reef banks, and atolls in the region. Here, we present baseline deep-sea coral species distribution and community assembly patterns within the Scleractinia, Octocorallia, Antipatharia, and Zoantharia with respect to different seafloor features and abiotic environmental variables across bathyal depths (200–2500 m). Remotely operated vehicle (ROV) transects were performed on 17 features throughout the Phoenix Islands and Tokelau Ridge Seamounts resulting in the observation of 12,828 deep-water corals and 167 identifiable morphospecies. Anthozoan assemblages were largely octocoral-dominated consisting of 78% of all observations with seamounts having a greater number of observed morphospecies compared to other feature types. Overlying water masses were observed to have significant effects on community assembly across bathyal depths. Revised species inventories further suggest that the protected area it is an area of biogeographic overlap for Pacific deep-water corals, containing species observed across bathyal provinces in the North Pacific, Southwest Pacific, and Western Pacific. These results underscore significant geographic and environmental complexity associated with deep-sea coral communities that remain in under-characterized in the equatorial central Pacific, but also highlight the additional efforts that need to be brought forth to effectively establish baseline ecological metrics in data deficient bathyal provinces.Funding for this work was provided by NOAA Office of Ocean Exploration and Research (Grant No. NA17OAR0110083) to RR, EC, TS, and David Gruber

Mind the gap: comparing exploration effort with global biodiversity patterns and climate projections to determine ocean areas with greatest exploration needs

The oceans contain 1,335 million km3 of water covering 361.9 million km2 of seafloor across 71% of the planet. In the past few decades, there has been substantial effort put into mapping and exploring the ocean fueled by the advent of new technologies that more easily enable deepwater access. However, we are still far from achieving our shared goals of a well characterized and documented ocean. In 2010, Webb et al. documented the paucity of deep-sea data in general, with a specific focus on the lack of pelagic records in the Ocean Biogeographic Information System OBIS, which is the largest of the ocean biodiversity archives. While significant exploration progress has been made, the rate of change in the ocean is outstripping the rate of characterization and research. Given the limited resources available, future work needs to be prioritized to focus on areas of greatest need. Here, we investigated several lines of inquiry to determine priority areas for future exploration. We accumulated the largest database of global deep submergence dive records ever compiled and used it, plus OBIS biodiversity records, to assess the level of exploration in different ocean regions. Then, we compared these measures of exploration effort with different biogeographic province schemas and estimates of climate change velocity projections to identify the largest remaining gaps in exploration and research sampling. Given that marine science has only explored between 5 and 20% of the ocean (depending on estimates) in the last hundred and fifty years, future exploration needs to be more targeted to attempt to keep pace with the rate and impact of environmental and biodiversity change in the ocean

Evidence and patterns of tuna spawning inside a large no-take marine protected area

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hernandez, C. M., Witting, J., Willis, C., Thorrold, S. R., Llopiz, J. K., & Rotjan, R. D. Evidence and patterns of tuna spawning inside a large no-take marine protected area. Scientific Reports, 9(1), (2019): 10772, doi:10.1038/s41598-019-47161-0.The Phoenix Islands Protected Area (PIPA), one of the world’s largest marine protected areas, represents 11% of the exclusive economic zone of the Republic of Kiribati, which earns much of its GDP by selling tuna fishing licenses to foreign nations. We have determined that PIPA is a spawning area for skipjack (Katsuwonus pelamis), bigeye (Thunnus obesus), and yellowfin (Thunnus albacares) tunas. Our approach included sampling larvae on cruises in 2015–2017 and using a biological-physical model to estimate spawning locations for collected larvae. Temperature and chlorophyll conditions varied markedly due to observed ENSO states: El Niño (2015) and neutral (2016–2017). However, larval tuna distributions were similar amongst years. Generally, skipjack larvae were patchy and more abundant near PIPA’s northeast corner, while Thunnus larvae exhibited lower and more even abundances. Genetic barcoding confirmed the presence of bigeye (Thunnus obesus) and yellowfin (Thunnus albacares) tuna larvae. Model simulations indicated that most of the larvae collected inside PIPA in 2015 were spawned inside, while stronger currents in 2016 moved more larvae across PIPA’s boundaries. Larval distributions and relative spawning output simulations indicated that both focal taxa spawned inside PIPA in all 3 study years, demonstrating that PIPA is protecting viable tuna spawning habitat.Funding and support was provided by the PIPA Trust, Waitt and Oceans5 Foundations, Sea Education Association, the Prince Albert of Monaco Foundation II, New England Aquarium, and Boston University to R.R. and J.W. C.H. was additionally supported by a National Science Foundation Graduate Research Fellowship. J.L. was additionally supported by NOAA through the Cooperative Institute for the North Atlantic Region (CINAR) under Cooperative Agreement NA14OAR4320158 in the form a CINAR Fellow Award, as well as by the WHOI Academic Programs Office. We thank A. Breef-Pilz for onboard sampling assistance, as well as S. Glancy, J. Pringle, E. Martin, J. Fisher, H. Goss, J. Jaskiel, S. Sheehan, and C. Moller for lab assistance. We thank the PIPA Trust and the PIPA Implementation Office for their support, as well as on-ship Kiribati Observers for their support and assistance: Tekeua Auatabu, Iannang Teaioro, Toaea Beiateuea, Taremon Korere, Kareati Waysang, and Moamoa Kabuati. We thank Q. Hanich for reading sections of this paper in advance. This research was conducted under Kiribati and PIPA permits PRP #s 3/17, 1/16, and 2/15 to JW

The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals

For animals that harbor photosynthetic symbionts within their tissues, such as corals, the different relative contributions of autotrophy versus heterotrophy to organismal energetic requirements have direct impacts on fitness. This is especially true for facultatively symbiotic corals, where the balance between host‐caught and symbiont‐produced energy can be altered substantially to meet the variable demands of a shifting environment. In this study, we utilized a temperate coral–algal system (the northern star coral, Astrangia poculata, and its photosynthetic endosymbiont, Symbiodinium psygmophilum) to explore the impacts of nutritional sourcing on the host's health and ability to regenerate experimentally excised polyps. For fed and starved colonies, wound healing and total colony tissue cover were differentially impacted by heterotrophy versus autotrophy. There was an additive impact of positive nutritional and symbiotic states on a coral's ability to initiate healing, but a greater influence of symbiont state on the recovery of lost tissue at the lesion site and complete polyp regeneration. On the other hand, regardless of symbiont state, fed corals maintained a higher overall colony tissue cover, which also enabled more active host behavior (polyp extension) and endosymbiont behavior (photosynthetic ability of Symbiondinium). Overall, we determined that the impact of nutritional state and symbiotic state varied between biological functions, suggesting a diversity in energetic sourcing for each of these processes.PADI Foundation; Cell Signaling Technologies; Boston University Marine Program Warren McLeod Fellowship; New England Aquarium; National Science Foundation, Grant/Award Number: IOS-1354935 (PADI Foundation; Cell Signaling Technologies; Boston University Marine Program Warren McLeod Fellowship; New England Aquarium; IOS-1354935 - National Science Foundation)Published versio

The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals

For animals that harbor photosynthetic symbionts within their tissues, such as corals, the different relative contributions of autotrophy versus heterotrophy to organismal energetic requirements have direct impacts on fitness. This is especially true for facultatively symbiotic corals, where the balance between host‐caught and symbiont‐produced energy can be altered substantially to meet the variable demands of a shifting environment. In this study, we utilized a temperate coral–algal system (the northern star coral, Astrangia poculata, and its photosynthetic endosymbiont, Symbiodinium psygmophilum) to explore the impacts of nutritional sourcing on the host's health and ability to regenerate experimentally excised polyps. For fed and starved colonies, wound healing and total colony tissue cover were differentially impacted by heterotrophy versus autotrophy. There was an additive impact of positive nutritional and symbiotic states on a coral's ability to initiate healing, but a greater influence of symbiont state on the recovery of lost tissue at the lesion site and complete polyp regeneration. On the other hand, regardless of symbiont state, fed corals maintained a higher overall colony tissue cover, which also enabled more active host behavior (polyp extension) and endosymbiont behavior (photosynthetic ability of Symbiondinium). Overall, we determined that the impact of nutritional state and symbiotic state varied between biological functions, suggesting a diversity in energetic sourcing for each of these processes.PADI Foundation; Cell Signaling Technologies; Boston University Marine Program Warren McLeod Fellowship; New England Aquarium; National Science Foundation, Grant/Award Number: IOS-1354935 (PADI Foundation; Cell Signaling Technologies; Boston University Marine Program Warren McLeod Fellowship; New England Aquarium; IOS-1354935 - National Science Foundation)Published versio

Free-Living Tube Worm Endosymbionts Found at Deep-Sea Vents

Recent evidence suggests that deep-sea vestimentiferan tube worms acquire their endosymbiotic bacteria from the environment each generation; thus, free-living symbionts should exist. Here, free-living tube worm symbiont phylotypes were detected in vent seawater and in biofilms at multiple deep-sea vent habitats by PCR amplification, DNA sequence analysis, and fluorescence in situ hybridization. These findings support environmental transmission as a means of symbiont acquisition for deep-sea tube worms.Organismic and Evolutionary Biolog

Deep-sea microbes as tools to refine the rules of innate immune pattern recognition.

The assumption of near-universal bacterial detection by pattern recognition receptors is a foundation of immunology. The limits of this pattern recognition concept, however, remain undefined. As a test of this hypothesis, we determined whether mammalian cells can recognize bacteria that they have never had the natural opportunity to encounter. These bacteria were cultivated from the deep Pacific Ocean, where the genus Moritella was identified as a common constituent of the culturable microbiota. Most deep-sea bacteria contained cell wall lipopolysaccharide (LPS) structures that were expected to be immunostimulatory, and some deep-sea bacteria activated inflammatory responses from mammalian LPS receptors. However, LPS receptors were unable to detect 80% of deep-sea bacteria examined, with LPS acyl chain length being identified as a potential determinant of immunosilence. The inability of immune receptors to detect most bacteria from a different ecosystem suggests that pattern recognition strategies may be defined locally, not globally.R01 AI093589 - NIAID NIH HHS; P30 DK034854 - NIDDK NIH HHS; U19 AI133524 - NIAID NIH HHS; R01 AI147314 - NIAID NIH HHS; R01 AI116550 - NIAID NIH HHS; R37 AI116550 - NIAID NIH HHS; R01 AI123820 - NIAID NIH HHSAccepted manuscrip

Genomic comparison of the temperate coral Astrangia poculata with tropical corals yields insights into winter quiescence, innate immunity, and sexual reproduction

Facultatively symbiotic corals provide important experimental models to explore the establishment, maintenance, and breakdown of the mutualism between corals and members of the algal family Symbiodiniaceae. The temperate coral Astrangia poculata is one such model as it is not only facultatively symbiotic, but also occurs across a broad temperature and latitudinal gradient. Here, we report the de novo chromosome-scale assembly and annotation of the A. poculata genome. Though widespread segmental/tandem duplications of genomic regions were detected, we did not find strong evidence of a whole genome duplication (WGD) event. Comparison of the gene arrangement between A. poculata and the tropical coral Acropora millepora revealed 56.38% of the orthologous genes were conserved in syntenic blocks despite ~415 million years of divergence. Gene families related to sperm hyperactivation and innate immunity, including lectins, were found to contain more genes in A. millepora relative to A. poculata. Sperm hyperactivation in A. millepora is expected given the extreme requirements of gamete competition during mass spawning events in tropical corals, while lectins are important in the establishment of coral-algal symbiosis. By contrast, gene families involved in sleep promotion, feeding suppression, and circadian sleep/wake cycle processes were expanded in A. poculata. These expanded gene families may play a role in A. poculata’s ability to enter a dormancy-like state (“winter quiescence”) to survive freezing temperatures at the northern edges of the species’ range.IOS-1354935 - National Science FoundationFirst author draf