Integrated physiological response by four species of Rhodophyta to submarine groundwater discharge reveals complex patterns among closely-related species.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 10 2024
09 10 2024
Historique:
received:
04
04
2023
accepted:
26
09
2024
medline:
10
10
2024
pubmed:
10
10
2024
entrez:
9
10
2024
Statut:
epublish
Résumé
Algal physiological ecology on submarine groundwater discharge (SGD) influenced reefs is likely shaped by intermittent, tidally-driven estuarine conditions that occur with SGD fluxes of fresh-to-brackish groundwater from the subterranean estuary to reef ecosystems. SGD is a common inconspicuous feature worldwide on reefs of basaltic high islands and continental margins. Yet, SGD-driven dynamics of algal physiology are not well understood. To understand how invasive species have physiologically outcompeted native species on many SGD-influenced reefs, physiology in tissue water potential (TWP) regulation, photosynthesis, nitrogen storage, and cellular anatomy were measured across a gradient of SGD-influence, for four Rhodophyte species. Compared with non-SGD conditions, SGD was associated with higher TWP, larger medulla cells with thinner walls, and thinner cortical cell walls for two invasives, Gracilaria salicornia and Acanthophora spicifera, higher photosynthetic rates in G. salicornia, greater nitrogen concentration for A. spicifera and G. salicornia, and increased
Identifiants
pubmed: 39384860
doi: 10.1038/s41598-024-74555-6
pii: 10.1038/s41598-024-74555-6
doi:
Substances chimiques
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
23547Informations de copyright
© 2024. The Author(s).
Références
Dimova, N. T., Swarzenski, P. W., Dulaiova, H. & Glenn, C. R. Utilizing multichannel electrical resistivity methods to examine the dynamics of the fresh water-seawater interface in two Hawaiian groundwater systems. J. Geophys. Res. Oceans. https://doi.org/10.1029/2011JC007509 (2012).
doi: 10.1029/2011JC007509
Smyth, K. & Elliott, M. Effects of changing salinity on the ecology of the marine environment. in Stressors in the Marine Environment: Physiological and Ecological Responses; Societal Implications, 161–174 (Oxford, 2016).
Elliott, M. & Quintino, V. The Estuarine Quality Paradox, Environmental Homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar. Pollut. Bull. 54, 640–645. https://doi.org/10.1016/j.marpolbul.2007.02.003 (2007).
doi: 10.1016/j.marpolbul.2007.02.003
Kirst, G. Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 21–53 (1989).
Dulai, H., Smith, C. M., Amato, D. W., Gibson, V. & Bremer, L. L. Risk to native marine macroalgae from land-use and climate change-related modifications to groundwater discharge in Hawai’i. Limnol. Oceanogr. Lett. https://doi.org/10.1002/lol2.10232 (2021).
doi: 10.1002/lol2.10232
Peterson, R. N., Burnett, W. C., Glenn, C. R. & Johnson, A. G. Quantification of point-source groundwater discharges to the ocean from the shoreline of the Big Island, Hawaii. Limnol. Oceanogr. 54, 890–904. https://doi.org/10.4319/lo.2009.54.3.0890 (2009).
doi: 10.4319/lo.2009.54.3.0890
Richardson, C. M., Dulai, H., Popp, B. N., Ruttenberg, K. & Fackrell, J. K. Submarine groundwater discharge drives biogeochemistry in two Hawaiian reefs. Limnol. Oceanogr. 62, S348–S363. https://doi.org/10.1002/lno.10654 (2017).
doi: 10.1002/lno.10654
Moosdorf, N., Stieglitz, T., Waska, H., Dürr, H. H. & Hartmann, J. Submarine groundwater discharge from tropical islands: A review. Grundwasser 20, 53–67. https://doi.org/10.1007/s00767-014-0275-3 (2015).
doi: 10.1007/s00767-014-0275-3
Haßler, K. et al. Provenance of nutrients in submarine fresh groundwater discharge on Tahiti and Moorea, French Polynesia. Appl. Geochem. 100, 181–189. https://doi.org/10.1016/j.apgeochem.2018.11.020 (2019).
doi: 10.1016/j.apgeochem.2018.11.020
Shuler, C. K. et al. Assessment of terrigenous nutrient loading to coastal ecosystems along a human land-use gradient, Tutuila, American Samoa. Hydrology 6, 18. https://doi.org/10.3390/hydrology6010018 (2019).
doi: 10.3390/hydrology6010018
Moore, W. S. The effect of submarine groundwater discharge on the ocean. Annu. Rev. Mar. Sci. 2, 59–88. https://doi.org/10.1146/annurev-marine-120308-081019 (2010).
doi: 10.1146/annurev-marine-120308-081019
Bratton, J. F. The three scales of submarine groundwater flow and discharge across passive continental margins. J. Geol. 118, 565–575. https://doi.org/10.1086/655114 (2010).
doi: 10.1086/655114
Beusen, A. H. W., Slomp, C. P. & Bouwman, A. F. Global land-ocean linkage: Direct inputs of nitrogen to coastal waters via submarine groundwater discharge. Environ. Res. Lett. 8, 034035. https://doi.org/10.1088/1748-9326/8/3/034035 (2013).
doi: 10.1088/1748-9326/8/3/034035
Knee, K. L., Street, J. H., Grossman, E. E., Boehm, A. B. & Paytan, A. Nutrient inputs to the coastal ocean from submarine groundwater discharge in a groundwater-dominated system: Relation to land use (Kona coast, Hawaii, U.S.A.). Limnol. Oceanogra. 55, 1105–1122. https://doi.org/10.4319/lo.2010.55.3.1105 (2010).
Valle, F. F. L., Thomas, F. I. & Nelson, C. E. Macroalgal biomass, growth rates, and diversity are influenced by submarine groundwater discharge and local hydrodynamics in tropical reefs. Mar. Ecol. Progress Series 621, 51–67. https://doi.org/10.3354/meps12992 (2019).
doi: 10.3354/meps12992
Amato, D. W., Bishop, J. M., Glenn, C. R., Dulai, H. & Smith, C. M. Impact of submarine groundwater discharge on marine water quality and reef biota of Maui. PLOS One 11, e0165825. https://doi.org/10.1371/journal.pone.0165825 (2016).
doi: 10.1371/journal.pone.0165825
pmcid: 5094668
Smith, J. E. et al. Ecology of the Invasive Red Alga Gracilaria salicornia (Rhodophyta) on O’ahu, Hawai’i. Pacific Sci. (2004).
Dailer, M. L., Knox, R. S., Smith, J. E., Napier, M. & Smith, C. M. Using δ
doi: 10.1016/j.marpolbul.2009.12.021
Costa, O. S., Nimmo, M. & Attrill, M. J. Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. J. S. Am. Earth Sci. 25, 257–270. https://doi.org/10.1016/j.jsames.2007.10.002 (2008).
doi: 10.1016/j.jsames.2007.10.002
Lyons, D. A. et al. Macroalgal blooms alter community structure and primary productivity in marine ecosystems. Glob. Change Biol. 20, 2712–2724. https://doi.org/10.1111/gcb.12644 (2014).
doi: 10.1111/gcb.12644
Delevaux, J. M. S. et al. A linked land-sea modeling framework to inform ridge-to-reef management in high oceanic islands. PLoS ONE. https://doi.org/10.1371/journal.pone.0193230 (2018).
doi: 10.1371/journal.pone.0193230
pmcid: 5851582
Brock, J. H. & Brock, R. E. The Marine Fauna Of The Coast of Northern Kona, Hawaii: An Inventory Of Fishes And Invertebrates Recorded During Summer, 1972 (University of Hawaii Sea Grant, 1974).
Biebl, R. Ecological and non- environmental constitutional resistance of the protoplasm of marine algae. J. Mar. Biol. Assoc. UK 31, 307–315 (1952).
doi: 10.1017/S0025315400053017
Amato, D. W., Smith, C. M. & Duarte, T. K. Submarine groundwater discharge differentially modifies photosynthesis, growth, and morphology for two contrasting species of Gracilaria (Rhodophyta). Hydrology 5, 65. https://doi.org/10.3390/hydrology5040065 (2018).
doi: 10.3390/hydrology5040065
Richards Donà, A., Smith, C. M. & Bremer, L. L. Divergent responses of native and invasive macroalgae to submarine groundwater discharge. Sci. Rep. 13, 13984. https://doi.org/10.1038/s41598-023-40854-7 (2023).
doi: 10.1038/s41598-023-40854-7
pmcid: 10460400
Reed, R. H. Use and abuse of osmo-terminology. Plant Cell Environ. 7, 165–170. https://doi.org/10.1111/1365-3040.ep11614591 (1984).
doi: 10.1111/1365-3040.ep11614591
Young, A. J., Collins, J. C. & Russel, G. Ecotypic variation in the osmotic responses of Enteromorpha intestinalis (L.) link. J. Exp. Bot. 38, 1309–1324. https://doi.org/10.1093/jxb/38.8.1309 (1987).
Zimmermann, U. Physics of turgor- and osmoregulation. Annu. Rev. Plant Physiol. 29, 121–148. https://doi.org/10.1146/annurev.pp.29.060178.001005 (1978).
doi: 10.1146/annurev.pp.29.060178.001005
Reed, R. H. Osmoacclimation in Bangia atropurpurea (Rhodophyta, Bangiales): The osmotic role of floridoside. Br. Phycol. J. 20, 211–218. https://doi.org/10.1080/00071618500650221 (1985).
doi: 10.1080/00071618500650221
Chardakov, V. New field method for the determination of the suction pressure of plants. Dokl. Akad. Nauk SSSR. 60 (1948).
O’Leary, J. W. A critical evaluation of tissue-immersion methods for measurement of plant water potential. Ohio J. Plant Sci. 70, 34–38 (1970).
Gibson, V. L., Richards Donà, A. & Smith, C. M. Measuring tissue water potential in marine macroalgae via an updated Chardakov method. AoB Plants. 15, plad055. https://doi.org/10.1093/aobpla/plad055 (2023).
Silbiger, N. J., Donahue, M. J. & Lubarsky, K. Submarine groundwater discharge alters coral reef ecosystem metabolism. Proc. R. Soc. B Biol. Sci. 287, 20202743. https://doi.org/10.1098/rspb.2020.2743 (2020).
doi: 10.1098/rspb.2020.2743
Abbott, I. A. Marine Red Algae of the Hawaiian Islands (Bishop Museum Pr, 1999).
Russell, D. J. The ecological invasion of Hawaiian reefs by two marine red algae, Acanthophora spicifera (Vahl) Boerg. and Hypnea musciformis (Wulfen) J. Ag., and their association with two native species, Laurencia nidifica J. Ag. and Hypnea cervicornis J. Ag. ICES Marine Science Symposium. 194 (1992).
Pereira, D. T. et al. Effects of salinity on the physiology of the red macroalga, Acanthophora spicifera (Rhodophyta, Ceramiales). Acta Botanica Brasilica 31, 555–565. https://doi.org/10.1590/0102-33062017abb0059 (2017).
doi: 10.1590/0102-33062017abb0059
Sherwood, A. R. & Guiry, M. D. Inventory of the seaweeds and seagrasses of the Hawaiian Islands. Biology. 12, 215. https://doi.org/10.3390/biology12020215 (2023).
doi: 10.3390/biology12020215
pmcid: 9953416
Oliveira, A. S., Sudatti, D. B., Fujii, M. T., Rodrigues, S. V. & Pereira, R. C. Inter- and intrapopulation variation in the defensive chemistry of the red seaweed Laurencia dendroidea (Ceramiales, Rhodophyta). Phycologia 52, 130–136. https://doi.org/10.2216/12-058.1 (2013).
doi: 10.2216/12-058.1
Sudatti, D. B. et al. Diel variation of sesquiterpene elatol production: A chemical defense mechanism of the red seaweed Laurencia dendroidea. Biochem. Syst. Ecol. 64, 131–135. https://doi.org/10.1016/j.bse.2015.12.001 (2016).
doi: 10.1016/j.bse.2015.12.001
Sudatti, D. B., Fujii, M. T., Rodrigues, S. V., Turra, A. & Pereira, R. C. Prompt induction of chemical defenses in the red seaweed Laurencia dendroidea: The role of herbivory and epibiosis. J. Sea Res. 138, 48–55. https://doi.org/10.1016/j.seares.2018.04.007 (2018).
doi: 10.1016/j.seares.2018.04.007
Conklin, K. Y., O’Doherty, D. C. & Sherwood, A. R. Hydropuntia perplexa, n. comb. (Gracilariaceae, Rhodophyta), First Record of the Genus in Hawai‘i1. Pacif. Sci. 68, 421–434. https://doi.org/10.2984/68.3.9 (2014).
Lyra, G. M. et al. Phylogenomics, divergence time estimation and trait evolution provide a new look into the Gracilariales (Rhodophyta). Mol. Phylogenet. Evolut. 165, 107294. https://doi.org/10.1016/j.ympev.2021.107294 (2021).
doi: 10.1016/j.ympev.2021.107294
Yokoya, N. S., West, J. A. & Luchi, A. E. Effects of plant growth regulators on callus formation, growth and regeneration in axenic tissue cultures of Gracilaria tenuistipitata and Gracilaria perplexa (Gracilariales, Rhodophyta). Phycol. Res. 52, 244–254. https://doi.org/10.1111/j.1440-183.2004.00349.x (2004).
doi: 10.1111/j.1440-183.2004.00349.x
Amato, D. W., Whittier, R. B., Dulai, H. & Smith, C. M. Algal bioassays detect modeled loading of wastewater-derived nitrogen in coastal waters of Oʻahu, Hawaiʻi. Mar. Pollut. Bull. 150, 110668. https://doi.org/10.1016/j.marpolbul.2019.110668 (2020).
doi: 10.1016/j.marpolbul.2019.110668
Gibson, V., Bremer, L., Burnett, K., Lui, N. & Smith, C. Biocultural values of groundwater dependent ecosystems in Kona, Hawai‘i. Ecol. Society. https://doi.org/10.5751/ES-13432-270318 (2022).
doi: 10.5751/ES-13432-270318
Alorda-Kleinglass, A. et al. The social implications of Submarine Groundwater Discharge from an Ecosystem Services perspective: A systematic review. Earth-Sci. Rev. 221, 103742. https://doi.org/10.1016/j.earscirev.2021.103742 (2021).
doi: 10.1016/j.earscirev.2021.103742
Moosdorf, N. & Oehler, T. Societal use of fresh submarine groundwater discharge: An overlooked water resource. Earth-Sci. Rev. 171, 338–348. https://doi.org/10.1016/j.earscirev.2017.06.006 (2017).
doi: 10.1016/j.earscirev.2017.06.006
McGaughey, S. A., Tyerman, S. D. & Byrt, C. S. An algal PIP-like aquaporin facilitates water transport and ionic conductance. Biochimica et Biophysica Acta (BBA) Biomembranes. 1863, 183661. https://doi.org/10.1016/j.bbamem.2021.183661 (2021).
Reed, R. H., Collins, J. C. & Russel, G. The effects of salinity upon cellular volume of the marine red alga Porphyra purpurea (Roth) C.Ag. J. Exp. Bot. 31, 1521–1537. https://doi.org/10.1093/jxb/31.6.1521 (1980).
McCook, L. J. Macroalgae, nutrients and phase shifts on coral reefs: Scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18, 357–367. https://doi.org/10.1007/s003380050213 (1999).
doi: 10.1007/s003380050213
Van Beukering, P. & Cesar, H. S. J. H. S. J. Ecological economic modeling of coral reefs: evaluating tourist overuse at Hanauma Bay and algae blooms at the Kihei Coast, Hawai‘i. Pacif. Sci. 58, 243–260. https://doi.org/10.1353/psc.2004.0012 (2004).
Nelson, C. E. et al. Fluorescent dissolved organic matter as a multivariate biogeochemical tracer of submarine groundwater discharge in coral reef ecosystems. Mar. Chem. 177, 232–243. https://doi.org/10.1016/j.marchem.2015.06.026 (2015).
doi: 10.1016/j.marchem.2015.06.026
Valle, F. F. L., Kantar, M. B. & Nelson, C. E. Coral reef benthic community structure is associated with the spatiotemporal dynamics of submarine groundwater discharge chemistry. Limnol. Oceanogr. https://doi.org/10.1002/lno.11596 (2020).
doi: 10.1002/lno.11596
Team, R. C. R version 4.1.3: A language and environment for statistical computing. (2022).
Bates, D. et al. lme4: Linear mixed-effects models using ‘Eigen’ and S4 (2022).
Bolker, B. M. Ecological Models and Data in R, 508th edn (Princeton University Press, 2008).
Fox, J. & Weisberg, S. An R Companion to Applied Regression. (SAGE Publications, 2018).
Pérez-Harguindeguy, N. et al. New handbook for standardised measurement of plant functional traits worldwide. Aust. J. Bot. 61, 167. https://doi.org/10.1071/BT12225 (2013).
doi: 10.1071/BT12225
Platt, T., Gallegos, C. L. & Harrison, W. G. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38 (1980).
Sigman, D. M. et al. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Analyt. Chem. 73, 4145–4153. https://doi.org/10.1021/ac010088e (2001).
doi: 10.1021/ac010088e
Tsuda, R. T., Fisher, J. R., Vroom, P. S. & Abbott, I. A. New records of subtidal benthic marine algae from Wake Atoll, Central Pacific. Botanica Marina 53, 19–29. https://doi.org/10.1515/BOT.2010.005 (2010).
doi: 10.1515/BOT.2010.005
Rasband, W. ImageJ (1997).
Doty, M. S. Acanthophora, a possible invader of the marine flora of Hawaii. Pacif. Sci. 15, 547–552 (1961).
O’Doherty, D. C. & Sherwood, A. R. Genetic population structure of the Hawaiian Alien invasive seaweed Acanthophora spicifera (Rhodophyta) as revealed by DNA sequencing and ISSR analyses. Pacif. Sci. 61, 223–233. https://doi.org/10.2984/1534-6188(2007)61[223:GPSOTH]2.0.CO;2 (2007).
doi: 10.2984/1534-6188(2007)61[223:GPSOTH]2.0.CO;2