{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T20:09:34Z","timestamp":1790107774113,"version":"4.0.1"},"reference-count":114,"publisher":"PeerJ","license":[{"start":{"date-parts":[[2022,2,9]],"date-time":"2022-02-09T00:00:00Z","timestamp":1644364800000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Songkla University and Ministry of Higher Education, Science, Research and Innovation under the Reinventing University Project","award":["REV64049"],"award-info":[{"award-number":["REV64049"]}]},{"name":"National Science, Research and Innovation Fund (NSRF) and Prince of Songkla University","award":["SCI6505095M"],"award-info":[{"award-number":["SCI6505095M"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:sec>\n<jats:title>Background<\/jats:title>\n<jats:p>The ability to maintain sufficient oxygen levels in the belowground tissues and the rhizosphere is crucial for the growth and survival of seagrasses in habitats with highly reduced sediment. Such ability varies depending on plant anatomical features and environmental conditions.<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>Methods<\/jats:title>\n<jats:p>In the present study, we compared anatomical structures of roots, rhizomes and leaves of the tropical intertidal seagrasses, <jats:italic>Cymodocea rotundata<\/jats:italic>, <jats:italic>Thalassia hemprichii<\/jats:italic> and <jats:italic>Halophila ovalis<\/jats:italic>, followed by an investigation of their gas exchange both in the belowground and aboveground tissues and photosynthetic electron transport rates (ETR) in response to experimental manipulations of O<jats:sub>2<\/jats:sub> level (normoxia and root hypoxia) and temperature (30 \u00b0C and 40 \u00b0C).<\/jats:p>\n<\/jats:sec>\n<jats:sec>\n<jats:title>Results<\/jats:title>\n<jats:p>We found that <jats:italic>C. rotundata<\/jats:italic> and <jats:italic>T. hemprichii<\/jats:italic> displayed mostly comparable anatomical structures, whereas <jats:italic>H. ovalis<\/jats:italic> displayed various distinctive features, including leaf porosity, number and size of lacunae in roots and rhizomes and structure of radial O<jats:sub>2<\/jats:sub> loss (ROL) barrier. <jats:italic>H. ovalis<\/jats:italic> also showed unique responses to root hypoxia and heat stress. Root hypoxia increased O<jats:sub>2<\/jats:sub> release from belowground tissues and overall photosynthetic activity of <jats:italic>H. ovalis<\/jats:italic> but did not affect the other two seagrasses. More pronounced warming effects were detected in <jats:italic>H. ovalis<\/jats:italic>, measured as lower O<jats:sub>2<\/jats:sub> release in the belowground tissues and overall photosynthetic capacity (O<jats:sub>2<\/jats:sub> release and dissolved inorganic carbon uptake in the light and ETR). High temperature inhibited photosynthesis of <jats:italic>C. rotundata<\/jats:italic> and <jats:italic>T. hemprichii<\/jats:italic> but did not affect their O<jats:sub>2<\/jats:sub> release in belowground tissues. Our data show that seagrasses inhabiting the same area respond differently to root hypoxia and temperature, possibly due to their differences in anatomical and physiological attributes. <jats:italic>Halophila ovalis<\/jats:italic> is highly dependent on photosynthesis and appears to be the most sensitive species with the highest tendency of O<jats:sub>2<\/jats:sub> loss in hypoxic sediment. At the same time, its root oxidation capacity may be compromised under warming scenarios.<\/jats:p>\n<\/jats:sec>","DOI":"10.7717\/peerj.12899","type":"journal-article","created":{"date-parts":[[2022,2,9]],"date-time":"2022-02-09T09:47:31Z","timestamp":1644400051000},"page":"e12899","source":"Crossref","is-referenced-by-count":5,"title":["Comparative study on anatomical traits and gas exchange responses due to belowground hypoxic stress and thermal stress in three tropical seagrasses"],"prefix":"10.7717","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4656-578X","authenticated-orcid":true,"given":"Sutthinut","family":"Soonthornkalump","sequence":"first","affiliation":[{"name":"Division of Biological Science, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand"},{"name":"Coastal Oceanography and Climate Change Research Center, Prince of Songkla University, Hat Yai, Songkhla, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan Xiang","family":"Ow","sequence":"additional","affiliation":[{"name":"St John\u2019s Island National Marine Laboratory, Tropical Marine Science Institute, National University of Singapore, Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chanida","family":"Saewong","sequence":"additional","affiliation":[{"name":"Division of Biological Science, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand"},{"name":"Coastal Oceanography and Climate Change Research Center, Prince of Songkla University, Hat Yai, Songkhla, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pimchanok","family":"Buapet","sequence":"additional","affiliation":[{"name":"Division of Biological Science, Faculty of Science, Prince of Songkla University, Hat Yai, Songkhla, Thailand"},{"name":"Coastal Oceanography and Climate Change Research Center, Prince of Songkla University, Hat Yai, Songkhla, Thailand"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4443","published-online":{"date-parts":[[2022,2,9]]},"reference":[{"issue":"1","key":"10.7717\/peerj.12899\/ref-1","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s10265-019-01150-6","article-title":"Aerenchyma and barrier to radial oxygen loss are formed in roots of Taro (Colocasia esculenta) propagules under flooded conditions","volume":"133","author":"Abiko","year":"2020","journal-title":"Journal of Plant Research"},{"key":"10.7717\/peerj.12899\/ref-2","doi-asserted-by":"publisher","first-page":"e892746","DOI":"10.1155\/2013\/892746","article-title":"The effects of water parameters on monthly seagrass percentage cover in Lawas, East Malaysia","volume":"2013","author":"Ahmad-Kamil","year":"2013","journal-title":"The Scientific World Journal"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-3","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.tree.2020.11.003","article-title":"Resilience of tropical ecosystems to ocean deoxygenation","volume":"36","author":"Altieri","year":"2021","journal-title":"Trends in Ecology & Evolution"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-4","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1111\/j.1399-3054.1971.tb01427.x","article-title":"Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging","volume":"25","author":"Armstrong","year":"1971","journal-title":"Physiologia Plantarum"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-5","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1006\/anbo.2000.1236","article-title":"Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis","volume":"86","author":"Armstrong","year":"2000","journal-title":"Annals of Botany"},{"key":"10.7717\/peerj.12899\/ref-6","doi-asserted-by":"publisher","first-page":"325","DOI":"10.3389\/fmars.2020.00325","article-title":"Morphological and physiological responses of Enhalus acoroides seedlings under varying temperature and nutrient treatment","volume":"7","author":"Artika","year":"2020","journal-title":"Frontiers in Marine Science"},{"issue":"1\u20136","key":"10.7717\/peerj.12899\/ref-7","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1515\/botm.1998.41.1-6.113","article-title":"Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance","volume":"41","author":"Beardall","year":"1998","journal-title":"Botanica Marina"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-8","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/S0304-3770(99)00020-0","article-title":"Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry","volume":"66","author":"Beer","year":"2000","journal-title":"Aquatic Botany"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-9","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1111\/j.1365-2745.2004.00943.x","article-title":"The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum","volume":"93","author":"Borum","year":"2005","journal-title":"Journal of Ecology"},{"key":"10.7717\/peerj.12899\/ref-10","first-page":"255","article-title":"Oxygen movement in seagrasses","volume-title":"Seagrasses: Biology, Ecologyconservation","author":"Borum","year":"2006"},{"key":"10.7717\/peerj.12899\/ref-11","doi-asserted-by":"publisher","first-page":"657","DOI":"10.3389\/fpls.2017.00657","article-title":"Sediment resuspension and deposition on seagrass leaves impedes internal plant aeration and promotes phytotoxic H2S intrusion","volume":"8","author":"Brodersen","year":"2017a","journal-title":"Frontiers in Plant Science"},{"issue":"7","key":"10.7717\/peerj.12899\/ref-12","doi-asserted-by":"publisher","first-page":"1619","DOI":"10.1111\/pce.12740","article-title":"Nanoparticle-based measurements of pH and O2 dynamics in the rhizosphere of Zostera marina L.: effects of temperature elevation and light-dark transitions","volume":"39","author":"Brodersen","year":"2016","journal-title":"Plant, Cell & Environment"},{"issue":"24","key":"10.7717\/peerj.12899\/ref-13","doi-asserted-by":"publisher","first-page":"14155","DOI":"10.1021\/acs.est.7b03878","article-title":"Seagrass-mediated phosphorus and iron solubilization in tropical sediments","volume":"51","author":"Brodersen","year":"2017b","journal-title":"Environmental Science &Technology"},{"key":"10.7717\/peerj.12899\/ref-14","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/978-3-319-71354-0_13","article-title":"Rhizome, Root\/sediment interactions, aerenchyma and internal pressure changes in seagrasses","volume-title":"Seagrasses of Australia: Structure, Ecology and Conservation","author":"Brodersen","year":"2018a"},{"issue":"64","key":"10.7717\/peerj.12899\/ref-15","doi-asserted-by":"publisher","first-page":"58","DOI":"10.3389\/fmars.2015.00058","article-title":"Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue","volume":"2","author":"Brodersen","year":"2015a","journal-title":"Frontiers in Marine Science"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-16","doi-asserted-by":"publisher","first-page":"1264","DOI":"10.1111\/nph.13124","article-title":"Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide","volume":"205","author":"Brodersen","year":"2015b","journal-title":"New Phytologist"},{"issue":"8","key":"10.7717\/peerj.12899\/ref-17","doi-asserted-by":"publisher","first-page":"2854","DOI":"10.1111\/1462-2920.14245","article-title":"Seagrass rhizosphere microenvironment alters plant-associated microbial community composition","volume":"20","author":"Brodersen","year":"2018b","journal-title":"Environmental Microbiology"},{"key":"10.7717\/peerj.12899\/ref-18","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.ecss.2017.09.034","article-title":"Recreating the shading effects of ship wake induced turbidity to test acclimation responses in the seagrass Thalassia hemprichii","volume":"199","author":"Browne","year":"2017","journal-title":"Estuarine Coastal and Shelf Science"},{"issue":"9","key":"10.7717\/peerj.12899\/ref-19","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1007\/s00227-017-3215-9","article-title":"Photosynthetic activity and photoprotection in green and red leaves of the seagrasses, Halophila ovalis and Cymodocea rotundata: implications for the photoprotective role of anthocyanin","volume":"164","author":"Buapet","year":"2017","journal-title":"Marine Biology"},{"issue":"11","key":"10.7717\/peerj.12899\/ref-20","doi-asserted-by":"publisher","first-page":"1040","DOI":"10.1071\/MF12124","article-title":"Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment","volume":"64","author":"Buapet","year":"2013","journal-title":"Marine and Freshwater Research"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-21","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/j.rse.2018.02.014","article-title":"Sea surface temperatures and seagrass mortality in Florida Bay: spatial and temporal patterns discerned from MODIS and AVHRR data","volume":"208","author":"Carlson","year":"2018","journal-title":"Remote Sensing of Environment"},{"key":"10.7717\/peerj.12899\/ref-22","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/s0022-0981(97)00084-1","article-title":"Leaf growth response to simulated herbivory: a comparison among seagrass species","volume":"220","author":"Cebri\u00e1n","year":"1998","journal-title":"Journal of Experimental Marine Biology and Ecology"},{"issue":"11","key":"10.7717\/peerj.12899\/ref-23","doi-asserted-by":"publisher","first-page":"1548","DOI":"10.1093\/treephys\/tpaa089","article-title":"Radial oxygen loss is correlated with nitrogen nutrition in mangroves","volume":"40","author":"Cheng","year":"2020a","journal-title":"Tree Physiology"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-24","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1007\/s10646-020-02221-4","article-title":"Dynamics of radial oxygen loss in mangroves subjected to waterlogging","volume":"29","author":"Cheng","year":"2020b","journal-title":"Ecotoxicology"},{"key":"10.7717\/peerj.12899\/ref-25","doi-asserted-by":"publisher","first-page":"355","DOI":"10.14456\/tjst.2020.25","article-title":"Comparative anatomy of two mangrove species, Xylocarpus granatum and Xylocarpus moluccensis (Meliaceae)","volume":"9","author":"Chorchuhirun","year":"2020","journal-title":"Thai Journal of Science and Technology"},{"key":"10.7717\/peerj.12899\/ref-26","doi-asserted-by":"publisher","first-page":"65","DOI":"10.3354\/meps07171","article-title":"Physiological characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability","volume":"353","author":"Collier","year":"2008","journal-title":"Marine Ecology Progress Series"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-27","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1016\/j.marpolbul.2014.03.050","article-title":"Temperature extremes reduce seagrass growth and induce mortality","volume":"83","author":"Collier","year":"2014","journal-title":"Marine Pollution Bulletin"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-28","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1046\/j.1365-3040.2003.00846.x","article-title":"Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots","volume":"26","author":"Colmer","year":"2003","journal-title":"Plant, Cell & Environment"},{"issue":"3\u20134","key":"10.7717\/peerj.12899\/ref-29","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/S0304-3770(98)00126-0","article-title":"Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination","volume":"63","author":"Connell","year":"1999","journal-title":"Aquatic Botany"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-30","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1016\/j.marpolbul.2017.04.013","article-title":"Phosphorus effects on radial oxygen loss, root porosity and iron plaque in two mangrove seedlings under cadmium stress","volume":"119","author":"Dai","year":"2017","journal-title":"Marine Pollution Bulletin"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-31","doi-asserted-by":"publisher","first-page":"105248","DOI":"10.1016\/j.marenvres.2020.105248","article-title":"Chlorophyll fluorescence, dark respiration and metabolomic analysis of Halodule pinifolia reveal potential heat responsive metabolites and biochemical pathways under ocean warming","volume":"164","author":"Danaraj","year":"2021","journal-title":"Marine Environmental Research"},{"issue":"321","key":"10.7717\/peerj.12899\/ref-32","doi-asserted-by":"publisher","first-page":"104169","DOI":"10.1016\/j.envexpbot.2020.104169","article-title":"The influence of dissolved oxygen around rice roots on salt tolerance during pre-tillering and tillering phases","volume":"178","author":"de Lopes","year":"2020","journal-title":"Environmental and Experimental Botany"},{"issue":"7","key":"10.7717\/peerj.12899\/ref-33","doi-asserted-by":"publisher","first-page":"880","DOI":"10.3390\/plants9070880","article-title":"Some accessions of Amazonian wild rice (Oryza glumaepatula) constitutively form a barrier to radial oxygen loss along adventitious roots under aerated conditions","volume":"9","author":"Ejiri","year":"2020","journal-title":"Plants"},{"key":"10.7717\/peerj.12899\/ref-34","doi-asserted-by":"publisher","first-page":"254","DOI":"10.3389\/fpls.2019.00254","article-title":"Prevention of radial oxygen loss is associated with exodermal suberin along adventitious roots of annual wild species of Echinochloa","volume":"10","author":"Ejiri","year":"2019","journal-title":"Frontiers in Plant Science"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-35","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/0304-3770(93)90065-5","article-title":"Primary production of seagrass beds in South Sulawesi (Indonesia): a comparison of habitats, methods and species","volume":"46","author":"Erftemeijer","year":"1993","journal-title":"Aquatic Botany"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-36","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.4319\/lo.2006.51.2.1072","article-title":"Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study","volume":"51","author":"Frederiksen","year":"2006","journal-title":"Limnology and Oceanography"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-37","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1007\/s13280-017-0916-8","article-title":"Seagrass metabolism and carbon dynamics in a tropical coastal embayment","volume":"46","author":"Ganguly","year":"2017","journal-title":"Ambio"},{"issue":"9","key":"10.7717\/peerj.12899\/ref-38","doi-asserted-by":"publisher","first-page":"4508","DOI":"10.1002\/ece3.3952","article-title":"High midday temperature stress has stronger effects on biomass than on photosynthesis: a mesocosm experiment on four tropical seagrass species","volume":"8","author":"George","year":"2018","journal-title":"Ecology and Evolution"},{"issue":"4","key":"10.7717\/peerj.12899\/ref-39","doi-asserted-by":"publisher","first-page":"1917","DOI":"10.1002\/ece3.6009","article-title":"Methane emission and sulfide levels increase in tropical seagrass sediments during temperature stress: a mesocosm experiment","volume":"10","author":"George","year":"2020","journal-title":"Ecology and Evolution"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-40","doi-asserted-by":"publisher","first-page":"210","DOI":"10.4319\/lo.2003.48.1.0210","article-title":"Meristematic oxygen variability in eelgrass (Zostera marina)","volume":"48","author":"Greve","year":"2003","journal-title":"Limnology and Oceanography"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-41","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.marpolbul.2016.08.084","article-title":"Individual and population indicators of Zostera japonica respond quickly to experimental addition of sediment-nutrient and organic matter","volume":"114","author":"Han","year":"2017","journal-title":"Marine Pollution Bulletin"},{"issue":"5","key":"10.7717\/peerj.12899\/ref-42","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1007\/s11306-015-0776-9","article-title":"Diurnal effects of anoxia on the metabolome of the seagrass Zostera marina","volume":"11","author":"Hasler-Sheetal","year":"2015","journal-title":"Metabolomics"},{"key":"10.7717\/peerj.12899\/ref-43","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511525551","volume-title":"Seagrass ecology","author":"Hemminga","year":"2000"},{"key":"10.7717\/peerj.12899\/ref-44","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1101\/2021.08.13.456246","article-title":"Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events","volume":"1","author":"Holmer","year":"2001","journal-title":"Aquatic Botany"},{"key":"10.7717\/peerj.12899\/ref-45","doi-asserted-by":"publisher","first-page":"2245","DOI":"10.1093\/jexbot\/52.365.2245","article-title":"The exodermis: a variable apoplastic barrier","volume":"52","author":"Hose","year":"2001","journal-title":"Journal of Experimental Botany"},{"key":"10.7717\/peerj.12899\/ref-46","doi-asserted-by":"publisher","first-page":"49","DOI":"10.3354\/meps293049","article-title":"Oxic microzones and radial oxygen loss from roots of Zostera marina","volume":"293","author":"Jensen","year":"2005","journal-title":"Marine Ecology Progress Series"},{"key":"10.7717\/peerj.12899\/ref-47","volume-title":"Plant microtechnique","author":"Johansen","year":"1940"},{"key":"10.7717\/peerj.12899\/ref-48","doi-asserted-by":"publisher","first-page":"95","DOI":"10.3354\/meps11041","article-title":"Rhizosphere O2 dynamics in young Zostera marina and Ruppia maritima","volume":"518","author":"Jovanovic","year":"2015","journal-title":"Marine Ecology Progress Series"},{"key":"10.7717\/peerj.12899\/ref-49","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.scitotenv.2015.04.061","article-title":"Unravelling complexity in seagrass systems for management: Australia as a microcosm","volume":"534","author":"Kilminster","year":"2015","journal-title":"The Science of the Total Environment"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-50","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/j.aquabot.2008.10.005","article-title":"Root architecture of six tropical seagrass species, growing in three contrasting habitats in Indonesian waters","volume":"90","author":"Kiswara","year":"2009","journal-title":"Aquatic Botany"},{"issue":"8","key":"10.7717\/peerj.12899\/ref-51","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1071\/MF19173","article-title":"Effects of shading on seagrass morphology and thermal optimal of productivity","volume":"71","author":"Kong","year":"2019","journal-title":"Marine and Freshwater Research"},{"key":"10.7717\/peerj.12899\/ref-52","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/978-3-319-71354-0_4","article-title":"Anatomy and structure of australian seagrasses","volume-title":"Seagrasses of Australia: Structure, Ecology and Conservation","author":"Kuo","year":"2018"},{"key":"10.7717\/peerj.12899\/ref-53","first-page":"51","article-title":"Seagrass morphology, anatomy, and ultrastructure","volume-title":"Seagrasses: Biology, Ecology and Conservation","author":"Kuo","year":"2006"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-54","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1515\/bot-2020-0079","article-title":"Effects of river water inflow on the growth, photosynthesis, and respiration of the tropical seagrass Halophila ovalis","volume":"64","author":"Lamit","year":"2021","journal-title":"Botanica Marina"},{"issue":"14","key":"10.7717\/peerj.12899\/ref-55","doi-asserted-by":"publisher","first-page":"3773","DOI":"10.1093\/jxb\/erx206","article-title":"Carbon-concentrating mechanisms in seagrasses","volume":"68","author":"Larkum","year":"2017","journal-title":"Journal of Experimental Botany"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-56","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1007\/s10452-012-9391-2","article-title":"The ability of aquatic macrophytes to increase root porosity and radial oxygen loss determines their resistance to sediment anoxia","volume":"2","author":"Lemoine","year":"2012","journal-title":"Aquatic Ecology"},{"issue":"9","key":"10.7717\/peerj.12899\/ref-57","doi-asserted-by":"publisher","first-page":"940","DOI":"10.1016\/j.tplants.2021.03.005","article-title":"How roots and shoots communicate through stressful times","volume":"26","author":"Li","year":"2021","journal-title":"Trends in Plant Science"},{"key":"10.7717\/peerj.12899\/ref-58","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.marpolbul.2017.09.005","article-title":"Shading and simulated grazing increase the sulphide pool and methane emission in a tropical seagrass meadow","volume":"134","author":"Lyimo","year":"2018","journal-title":"Marine Pollution Bulletin"},{"key":"10.7717\/peerj.12899\/ref-59","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/978-3-319-93594-2_11","article-title":"Trade-offs and synergies in the structural and functional characteristics of leaves photosynthesizing in aquatic environments","volume-title":"The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration","author":"Maberly","year":"2018"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-60","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/s41396-018-0308-5","article-title":"Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress","volume":"13","author":"Martin","year":"2019","journal-title":"The ISME Journal"},{"issue":"S1","key":"10.7717\/peerj.12899\/ref-61","doi-asserted-by":"publisher","first-page":"S381","DOI":"10.1002\/lno.10746","article-title":"Colonizing tropical seagrasses increase root exudation under fluctuating and continuous low light","volume":"63","author":"Martin","year":"2018","journal-title":"Limnology and Oceanography"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-62","doi-asserted-by":"publisher","first-page":"28615","DOI":"10.1038\/srep28615","article-title":"Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses","volume":"6","author":"Mar\u00edn-Guirao","year":"2016","journal-title":"Scientific Reports"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-63","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1111\/pce.12163","article-title":"Stomata actively regulate internal aeration of the sacred lotus Nelumbo nucifera","volume":"37","author":"Matthews","year":"2014","journal-title":"Plant, Cell & Environment"},{"issue":"1\u20132","key":"10.7717\/peerj.12899\/ref-64","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1007\/s11104-020-04634-w","article-title":"Effects of cultivars, water regimes, and growth stages on cadmium accumulation in rice with different radial oxygen loss","volume":"453","author":"Mei","year":"2020","journal-title":"Plant and Soil"},{"key":"10.7717\/peerj.12899\/ref-65","doi-asserted-by":"publisher","first-page":"812","DOI":"10.3389\/fmars.2019.00812","article-title":"Responses of invasive and native populations of the seagrass halophila stipulacea to simulated climate change","volume":"6","author":"Nguyen","year":"2020","journal-title":"Frontiers in Marine Science"},{"issue":"5","key":"10.7717\/peerj.12899\/ref-66","doi-asserted-by":"publisher","first-page":"2009","DOI":"10.1111\/brv.12736","article-title":"Seagrasses in an era of ocean warming: a review","volume":"96","author":"Nguyen","year":"2021","journal-title":"Biological Reviews of the Cambridge Philosophical Society"},{"key":"10.7717\/peerj.12899\/ref-67","first-page":"858","article-title":"Submerged aquatic vegetation: seagrasses","volume-title":"Encyclopedia of Natural Resources-Water and Air","volume":"II","author":"Novak","year":"2014"},{"key":"10.7717\/peerj.12899\/ref-68","doi-asserted-by":"publisher","first-page":"67","DOI":"10.3354\/meps12477","article-title":"In situ oxygen dynamics in rhizomes of the seagrass Posidonia sinuosa: impact of light, water column oxygen, current speed and wave velocity","volume":"590","author":"Olsen","year":"2018","journal-title":"Marine Ecology-Progress Series"},{"key":"10.7717\/peerj.12899\/ref-69","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1038\/nature16548","article-title":"The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea","volume":"530","author":"Olsen","year":"2016","journal-title":"Nature"},{"issue":"8","key":"10.7717\/peerj.12899\/ref-70","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1071\/MF19178","article-title":"Contribution of epiphyte load to light attenuation on seagrass leaves is small but critical in turbid waters","volume":"71","author":"Ow","year":"2020","journal-title":"Marine and Freshwater Research"},{"key":"10.7717\/peerj.12899\/ref-71","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1016\/j.marpolbul.2017.09.006","article-title":"Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance","volume":"134","author":"O\u2019Brien","year":"2018","journal-title":"Marine Pollution Bulletin"},{"key":"10.7717\/peerj.12899\/ref-72","doi-asserted-by":"publisher","first-page":"e103892","DOI":"10.5402\/2012\/103892","article-title":"Highlights in seagrasses\u2019 phylogeny, physiology, and metabolism: What makes them special?","volume":"2012","author":"Papenbrock","year":"2012","journal-title":"ISRN Botany"},{"key":"10.7717\/peerj.12899\/ref-73","doi-asserted-by":"publisher","first-page":"e0156214","DOI":"10.1371\/journal.pone.0156214","article-title":"Photoacclimatory responses of Zostera marina in the intertidal and subtidal zones","volume":"11","author":"Park","year":"2016","journal-title":"PLOS ONE"},{"key":"10.7717\/peerj.12899\/ref-74","doi-asserted-by":"publisher","first-page":"283","DOI":"10.3354\/meps169283","article-title":"Oxygen dynamics in the rhizosphere of Cymodocea rotundata","volume":"169","author":"Pedersen","year":"1998","journal-title":"Marine Ecology Progress Series"},{"issue":"4","key":"10.7717\/peerj.12899\/ref-75","doi-asserted-by":"publisher","first-page":"1207","DOI":"10.1111\/nph.13900","article-title":"Heat stress of two tropical seagrass species during low tides-impact on underwater net photosynthesis, dark respiration and diel in situ internal aeration","volume":"210","author":"Pedersen","year":"2016","journal-title":"The New Phytologist"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-76","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1111\/nph.16375","article-title":"Regulation of root adaptive anatomical and morphological traits during low soil oxygen","volume":"229","author":"Pedersen","year":"2021","journal-title":"New Phytologist"},{"key":"10.7717\/peerj.12899\/ref-77","doi-asserted-by":"publisher","first-page":"104267","DOI":"10.1016\/j.envexpbot.2020.104267","article-title":"Effect of sulfide and the role of root mass on metabolic fluxes in the seagrass Zostera marina","volume":"180","author":"Peyer","year":"2020","journal-title":"Environmental and Experimental Botany"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-78","doi-asserted-by":"publisher","first-page":"196","DOI":"10.3390\/biology1020196","article-title":"Soil oxidation-reduction in wetlands and its impact on plant functioning","volume":"1","author":"Pezeshki","year":"2012","journal-title":"Biology"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-79","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1515\/bot-2017-0084","article-title":"Photosynthetic and antioxidant responses of the tropical intertidal seagrasses Halophila ovalis and Thalassia hemprichii to moderate and high irradiances","volume":"61","author":"Phandee","year":"2018","journal-title":"Botanica Marina"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-80","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1016\/j.aquabot.2008.10.002","article-title":"Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species","volume":"90","author":"Pi","year":"2009","journal-title":"Aquatic Botany"},{"key":"10.7717\/peerj.12899\/ref-81","first-page":"1825","article-title":"Effect of high temperature stress on changes in morphology, anatomy and chlorophyll content in tropical seagrass Thalassia hemprichii","volume":"11","author":"Purnama","year":"2018","journal-title":"AACL Bioflux"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-82","doi-asserted-by":"publisher","first-page":"2056","DOI":"10.1093\/icesjms\/fsaa093","article-title":"Effects of temperature and hypoxia on respiration, photorespiration, and photosynthesis of seagrass leaves from contrasting temperature regimes","volume":"77","author":"Rasmusson","year":"2020","journal-title":"ICES Journal of Marine Science"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-83","doi-asserted-by":"publisher","first-page":"12667","DOI":"10.1038\/s41598-019-49184-z","article-title":"Estimation of a whole plant Q10 to assess seagrass productivity during temperature shifts","volume":"9","author":"Rasmusson","year":"2019","journal-title":"Scientific Report"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-84","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1007\/s00227-017-3168-z","article-title":"Respiratory oxygen consumption in the seagrass Zostera marina varies on a diel basis and is partly affected by light","volume":"164","author":"Rasmusson","year":"2017","journal-title":"Marine Biology"},{"issue":"16","key":"10.7717\/peerj.12899\/ref-85","doi-asserted-by":"publisher","first-page":"9433","DOI":"10.3390\/su13169433","article-title":"Sensitivity of photosynthesis to warming in two similar species of the aquatic Angiosperm Ruppia from tropical and temperate habitats","volume":"13","author":"Rasmusson","year":"2021","journal-title":"Sustainability"},{"issue":"4","key":"10.7717\/peerj.12899\/ref-86","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1016\/0304-3770(84)90058-5","article-title":"The structure and continuity of the lacunar system of the seagrass Halophila ovalis (R. Br.) Hook f. (Hydrocharitaceae)","volume":"18","author":"Roberts","year":"1984","journal-title":"Aquatic Botany"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-87","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1111\/j.1469-8137.1985.tb02754.x","article-title":"Root development in the seagrass Halophila ovalis (R. Br.) Hook F. (Hydrocharitaceae), with particular reference to root lacunae","volume":"100","author":"Roberts","year":"1985","journal-title":"New Phytologist"},{"key":"10.7717\/peerj.12899\/ref-88","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1111\/1365-2745.13479","article-title":"A king and vassals\u2019 tale: molecular signatures of clonal integration in Posidonia oceanica under chronic light shortage","volume":"109","author":"Roucco","year":"2020"},{"key":"10.7717\/peerj.12899\/ref-89","volume-title":"Plant microtechnique and microscopy","author":"Ruzin","year":"1999"},{"issue":"5","key":"10.7717\/peerj.12899\/ref-90","doi-asserted-by":"publisher","first-page":"247","DOI":"10.3109\/10520297309116632","article-title":"Simple method for differential staining of paraffin embedded plant material using toluidine blue O","volume":"48","author":"Sakai","year":"1973","journal-title":"Stain Technology"},{"issue":"4","key":"10.7717\/peerj.12899\/ref-91","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1093\/aob\/mci214","article-title":"Contrasting oxygen dynamics in the freshwater Isoetid Lobelia dortmanna and the marine seagrass Zostera marina","volume":"96","author":"Sand-Jensen","year":"2005","journal-title":"Annals of Botany"},{"issue":"3","key":"10.7717\/peerj.12899\/ref-92","doi-asserted-by":"publisher","first-page":"349","DOI":"10.2307\/3544675","article-title":"Oxygen release from roots of submerged aquatic macrophytes","volume":"38","author":"Sand-Jensen","year":"1982","journal-title":"Oikos"},{"key":"10.7717\/peerj.12899\/ref-93","first-page":"341","article-title":"Biodiversity of benthic fauna in the seagrass ecosystem of Kung Krabaen Bay, Chantaburi Province, Thailand","volume":"33","author":"Satumanatpan","year":"2011","journal-title":"Songklanakarin Journal of Science and Technology"},{"issue":"5","key":"10.7717\/peerj.12899\/ref-94","doi-asserted-by":"publisher","first-page":"2138","DOI":"10.1111\/nph.17415","article-title":"Cable bacteria at oxygen-releasing roots of aquatic plants: a widespread and diverse plant\u2013microbe association","volume":"232","author":"Scholz","year":"2021","journal-title":"New Phytologist"},{"key":"10.7717\/peerj.12899\/ref-95","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.marenvres.2018.02.008","article-title":"Contrasting impacts of light reduction on sediment biogeochemistry in deep- and shallow-water tropical seagrass assemblages (Green Island, Great Barrier Reef)","volume":"136","author":"Schrameyer","year":"2018","journal-title":"Marine Environmental Research"},{"key":"10.7717\/peerj.12899\/ref-96","doi-asserted-by":"publisher","first-page":"14825","DOI":"10.1038\/s41598-018-33259-4","article-title":"Photoacclimation strategies in northeastern Atlantic seagrasses: Integrating responses across plant organizational levels","volume":"8","author":"Schubert","year":"2018","journal-title":"Scientific Reports"},{"key":"10.7717\/peerj.12899\/ref-97","first-page":"146","article-title":"The Polychaeta (Annelida) communities of the Merambong and Tanjung Adang Shoals, Malaysia, and its relationship with the environmental variables","volume":"66","author":"Shi","year":"2015","journal-title":"Malayan Nature Journal"},{"key":"10.7717\/peerj.12899\/ref-98","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/B978-044450891-1\/50009-8","article-title":"Methods for the measurement of seagrass growth and production","volume-title":"Global seagrass research methods","author":"Short","year":"2001"},{"issue":"1,2","key":"10.7717\/peerj.12899\/ref-99","doi-asserted-by":"publisher","first-page":"67","DOI":"10.3233\/JCC-150005","article-title":"Seagrass ecosystem and climate change: an Indian perspective","volume":"1","author":"Singh","year":"2015","journal-title":"Journal of Climate Change"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-100","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1046\/j.0028-646X.2001.00317.x","article-title":"Development of anatomical structure of roots of Phragmites australis","volume":"153","author":"Soukup","year":"2002","journal-title":"New Phytologist"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-101","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.jembe.2014.12.014","article-title":"Prolonged buoyancy and viability of Zostera muelleri Irmisch ex Asch. vegetative fragments indicate a strong dispersal potential","volume":"464","author":"Stafford-Bell","year":"2015","journal-title":"Journal of Experimental Marine Biology and Ecology"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-102","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1111\/j.1469-8137.2010.03496.x","article-title":"Aerenchyma formation in the rice stem and its promotion by H2O2","volume":"190","author":"Steffens","year":"2011","journal-title":"The New Phytologist"},{"issue":"6","key":"10.7717\/peerj.12899\/ref-103","doi-asserted-by":"publisher","first-page":"3525","DOI":"10.1111\/gcb.15065","article-title":"Too hot to handle: unprecedented seagrass death driven by marine heatwave in a world heritage area","volume":"26","author":"Strydom","year":"2020","journal-title":"Global Change Biology"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-104","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1007\/s12562-009-0064-6","article-title":"The structural and histochemical analyses and chemical characters of the cuticle and epidermal walls of cotyledon in ungerminated seeds of Zostera marina L","volume":"75","author":"Sugiura","year":"2009","journal-title":"Fisheries Science"},{"issue":"4","key":"10.7717\/peerj.12899\/ref-105","doi-asserted-by":"publisher","first-page":"e10962","DOI":"10.7717\/peerj.10962","article-title":"Comparative anatomy and salt management of Sonneratia caseolaris (L.) Engl. (Lythraceae) grown in saltwater and freshwater","volume":"9","author":"Tatongjai","year":"2021","journal-title":"PeerJ"},{"issue":"1\u20134","key":"10.7717\/peerj.12899\/ref-106","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/S0304-3770(99)00039-X","article-title":"Are seagrass growth and survival constrained by the reducing conditions of the sediment?","volume":"65","author":"Terrados","year":"1999","journal-title":"Aquatic Botany"},{"issue":"5","key":"10.7717\/peerj.12899\/ref-107","doi-asserted-by":"publisher","first-page":"1182","DOI":"10.1007\/s12237-012-9514-y","article-title":"Temperature dependence of oxygen dynamics and community metabolism in a shallow Mediterranean macroalgal meadow (Caulerpa prolifera)","volume":"35","author":"Vaquer-Sunyer","year":"2012","journal-title":"Estuaries and Coasts"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-108","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1023\/A:1024560322835","article-title":"Measurement of porosity in very small samples of plant tissue","volume":"253","author":"Visser","year":"2003","journal-title":"Plant and Soil"},{"issue":"11","key":"10.7717\/peerj.12899\/ref-109","doi-asserted-by":"publisher","first-page":"1237","DOI":"10.1046\/j.1365-3040.2000.00628.x","article-title":"Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma","volume":"23","author":"Visser","year":"2000","journal-title":"Plant, Cell & Environment"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-110","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1016\/j.marpolbul.2013.11.030","article-title":"Chronic light reduction reduces overall resilience to additional shading stress in the seagrass Halophila ovalis","volume":"83","author":"Yaakub","year":"2014","journal-title":"Marine Pollution Bulletin"},{"issue":"1","key":"10.7717\/peerj.12899\/ref-111","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1007\/s10872-005-0030-6","article-title":"Quality of the seagrass Halophila ovalis on a Thai intertidal flat as food for the dugong","volume":"61","author":"Yamamuro","year":"2005","journal-title":"Journal of Oceanography"},{"issue":"2","key":"10.7717\/peerj.12899\/ref-112","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.1104\/pp.17.01157","article-title":"Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress","volume":"176","author":"Yamauchi","year":"2018","journal-title":"Plant Physiology"},{"key":"10.7717\/peerj.12899\/ref-113","doi-asserted-by":"publisher","first-page":"767628","DOI":"10.3389\/fmars.2021.767628","article-title":"Experimental assessment of vulnerability to warming in tropical shallow-water marine organisms","volume":"8","author":"Yucharoen","year":"2021","journal-title":"Frontiers in Marine Science"},{"key":"10.7717\/peerj.12899\/ref-114","doi-asserted-by":"publisher","first-page":"144717","DOI":"10.1016\/j.scitotenv.2020.144717","article-title":"New insights into physiological effects of anoxia under darkness on the iconic seagrass Zostera marina based on a combined analysis of transcriptomics and metabolomics","volume":"768","author":"Zhang","year":"2021","journal-title":"The Science of the Total Environment"}],"container-title":["PeerJ"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/peerj.com\/articles\/12899.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/12899.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/12899.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/peerj.com\/articles\/12899.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,9]],"date-time":"2022-02-09T09:47:55Z","timestamp":1644400075000},"score":1,"resource":{"primary":{"URL":"https:\/\/peerj.com\/articles\/12899"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,9]]},"references-count":114,"alternative-id":["10.7717\/peerj.12899"],"URL":"https:\/\/doi.org\/10.7717\/peerj.12899","archive":["CLOCKSS","LOCKSS","Portico"],"relation":{},"ISSN":["2167-8359"],"issn-type":[{"value":"2167-8359","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,9]]},"article-number":"e12899"}}