Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T10:55:54.891Z Has data issue: false hasContentIssue false

6 - The Evolution of Aquatic Embryophytes: Secondary Colonisers of Aquatic Environments

from Part I - Origins and Consequences of Early Photosynthetic Organisms

Published online by Cambridge University Press:  24 October 2024

By
Stephen C. Maberly
Edited by
Mario Giordano ,
John Beardall ,
John A. Raven  and
Stephen C. Maberly
Mario Giordano
Affiliation:
Università degli Studi di Ancona, Italy
John Beardall
Affiliation:
Monash University, Victoria
John A. Raven
Affiliation:
University of Dundee
Stephen C. Maberly
Affiliation:
UK Centre for Ecology & Hydrology, Lancaster
Get access

Summary

Seagrasses in marine systems and freshwater plants (macrophytes) in inland waters are important primary producers that structure their local ecosystems. They comprise the embryophytes: bryophytes, pteridophytes and angiosperms. They have adapted the genetic heritage of their land plant ancestors in response to the opportunities and challenges of life underwater. This has involved a reduction in the structures and processes required to manage: water content, the low physical support in air and the high levels of UV radiation. In contrast, inorganic carbon can restrict photosynthesis underwater but can be minimised by growing in sites with high CO2 concentrations, exploiting CO2 in the air or sediment and by CO2 concentrating mechanisms that rely on bicarbonate uptake, C4 photosynthesis or Crassulacean acid metabolism. Most aquatic embryophytes are, like their terrestrial ancestors, rhizophytic, allowing nutrients to be taken up from both the sediment and water. Some, especially the bryophytes, are haptophytic and only obtain nutrients from the water column.

Keywords

C3 photosynthesisC4 photosynthesiscarbon-concentrating mechanismcarbonic anhydraseCrassulacean acid metabolismhaptophytemacrophyterhizophyteseagrass
Type
Chapter
Information
Evolutionary Physiology of Algae and Aquatic Plants , pp. 96 - 112
Publisher: Cambridge University Press
Print publication year: 2024

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albayrak, I., Nikora, V., Miler, O. et al. (2012). Flow-plant interactions at a leaf scale: Effects of leaf shape, serration, roughness and flexural rigidity. Aquatic Sciences 74: 267–286.CrossRefGoogle Scholar
Aulio, K. (1985). Differential expression of diel acid metabolism in two life forms of Littorella uniflora (L.) Aschers. New Phytologist 100: 533–536.CrossRefGoogle Scholar
Bagger, J. & Madsen, T. V. (2004). Morphological acclimation of aquatic Littorella uniflora to sediment CO2 concentration and wave exposure. Functional Ecology 18: 946–951.CrossRefGoogle Scholar
Binzer, T., Sand-Jensen, K. & Middelboe, A.-L. (2006). Community photosynthesis of aquatic macrophytes. Limnology and Oceanography 51: 2722–2733.CrossRefGoogle Scholar
Black, C. C. & Osmond, C. B. (2003). Crassulacean acid metabolism: ‘Working the night shift’. Photosynthesis Research 76: 329–341.CrossRefGoogle ScholarPubMed
Borum, J., Pedersen, O., Kotula, L. et al. (2016). Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant Cell and Environment 39: 1240–1250.CrossRefGoogle ScholarPubMed
Bowes, G., Rao, S. K., Estavillo, G. M. et al. (2002). C4 mechanisms in aquatic angiosperms: Comparisons with terrestrial C4 systems. Functional Plant Biology 29: 379–392.CrossRefGoogle ScholarPubMed
Bräutigam, A., Schliesky, S., Kuelahoglu, C. et al. (2014). Towards an integrative model of C4 photosynthetic subtypes: Insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. Journal of Experimental Botany 65: 3579–3593.CrossRefGoogle ScholarPubMed
Carr, H. & Axelsson, L. (2008). Photosynthetic utilization of bicarbonate in Zostera marina is reduced by inhibitors of mitochondrial ATPase and electron transport. Plant Physiology 147: 879–885.CrossRefGoogle ScholarPubMed
Casati, P., Lara, M. V. & Andreo, C. S. (2000). Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submersed aquatic species. Plant Physiology 123: 1611–1621.CrossRefGoogle Scholar
Chambers, P. A. & Maberly, S. C. (2023). Freshwater plants. In: Jones, I. D. and Smol, J. P. (eds.) Wetzel’s Limnology: Lake and River Ecosystems. Academic Press, Amsterdam, pp. 759–816.Google Scholar
Chen, L. Y., Chen, J. M., Gituru, R. W. et al. (2012). Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evolutionary Biology 12: 30. https://doi.org/10.1186/1471–2148–12–30.CrossRefGoogle ScholarPubMed
Christenhusz, M. J. M. & Byng, J. W. (2016). The number of known plants species in the world and its annual increase. Phytotaxa 261: 201–207.CrossRefGoogle Scholar
Christin, P.-A., Besnard, G., Samaritani, E. et al. (2008). Oligocene CO2 decline promoted C4 photosynthesis in grasses. Current Biology 18: 37–43.CrossRefGoogle ScholarPubMed
Cox, C., Goffinet, B., Wickett, N. et al. (2010). Moss diversity: A molecular phylogenetic analysis of genera. Phytotaxa 9: 175–195.CrossRefGoogle Scholar
Crandall-Stotler, B., Stotler, R. E. & Long, D. G. (2009). Phylogeny and classification of the Marchantiophyta. Edinburgh Journal of Botany 66: 155–198.CrossRefGoogle Scholar
den Hartog, C. & Kuo, J. (2006). Taxonomy and biogeography of seagrasses. In: Larkum, A. W. D., Orth, R. J. & Duarte, C. M. (eds.) Seagrasses: Biology, Ecology and Conservation. Springer, Dordrecht, The Netherlands, pp. 1–23.Google Scholar
den Hartog, C. & Triest, L. (2020). A profound view and discourse on the typification and status of three confused taxa: Ruppia maritima, R. spiralis and R. cirrhosa. Botanica Marina 63: 229–239.CrossRefGoogle Scholar
Denny, M. W. (1993). Air and Water: The Biology and Physics of Life’s Media, Princeton University Press, Princeton, NJ.CrossRefGoogle Scholar
Du, Z.-Y. & Wang, Q.-F. (2014). Correlations of life form, pollination mode and sexual system in aquatic angiosperms. PLOS ONE 9: e115653.CrossRefGoogle ScholarPubMed
Duarte, C. M. (2016). Reviews and syntheses: Hidden Forests, the role of vegetated coastal habitats on the ocean carbon budget. Biogeosciences 14: 301–310.CrossRefGoogle Scholar
Duarte, C. M., Losada, I. J., Hendriks, I. E. et al. (2013). The role of coastal plant communities for climate change mitigation and adaptation. Nature Climate Change 3: 961–968.CrossRefGoogle Scholar
Edwards, E. J. (2019). Evolutionary trajectories, accessibility and other metaphors: The case of C4 and CAM photosynthesis. New Phytologist 223: 1742–1755.CrossRefGoogle ScholarPubMed
Enriquez, S. (2005). Light absorption efficiency and the package effect in the leaves of the seagrass Thalassia testudinum. Marine Ecology Progress Series 289: 141–150.CrossRefGoogle Scholar
Friis, E. M., Pedersen, K. R. & Crane, P. R. (2001). Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 410: 357–360.CrossRefGoogle ScholarPubMed
Frost-Christensen, H., Jørgensen, L. B. & Floto, F. (2003). Species specificity of resistance to oxygen diffusion in thin cuticular membranes from amphibious plants. Plant Cell and Environment 26: 561–569.CrossRefGoogle Scholar
Glime, J. M. (2021). Aquatic and wet anthocerotophyta. In Bryophyte Ecology, Vol. 4. Habitats and roles, eBook available at http://digitalcommons.mtu.edu/bryophyte-ecology.Google Scholar
Gomez, B., Daviero-Gomez, V., Coiffard, C. et al. (2015). Montsechia, an ancient aquatic angiosperm. Proceedings of the National Academy of Sciences USA 112: 10985–10988.CrossRefGoogle ScholarPubMed
Gontero, B. & Maberly, S. C. (2022). Biochemical carbon dioxide concentrating mechanisms. In: Maberly, S. C. & Gontero, B. (eds.) Blue Planet, Red and Green Photosynthesis: Productivity and Carbon Cycling in Aquatic Ecosystems. ISTE-Wiley, London, pp. 133–166.CrossRefGoogle Scholar
Graham, L., Lewis, L. A., Taylor, W. et al. (2014). Early terrestrialization: Transition from algal to bryophyte grade. In: Hanson, D. T. & Rice, S. K. (eds.) Photosynthesis in Bryophytes and Early Land Plants, Vol. 37. Springer Science +Business Media, Dordercht, The Netherlands, pp. 9–28.CrossRefGoogle Scholar
Griffiths, H. (1992). Carbon isotope discrimination and the integration of carbon assimilation pathways in terrestrial CAM plants. Plant, Cell and Environment 15: 1051–1062.CrossRefGoogle Scholar
Hetherington, A. J., DiMichele, W. A., Lucas, S. G. et al. (2019). Tiny Rhizomorphic Rooting Systems from the Early Permian Abo Formation of New Mexico, USA. International Journal of Plant Sciences 180: 504–512.CrossRefGoogle Scholar
Hilt, S., Brothers, S., Jeppesen, E. et al. (2017). Translating regime shifts in shallow lakes into changes in ecosystem functions and services. BioScience 67: 928–936.CrossRefGoogle Scholar
Holaday, A. S. & Bowes, G. (1980). C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiology 65: 331–335.CrossRefGoogle Scholar
Huang, W., Han, S., Jiang, H. et al. (2020a). External α-carbonic anhydrase and solute carrier 4 are required for bicarbonate uptake in a freshwater angiosperm. Journal of Experimental Botany 71: 6004–6014.CrossRefGoogle Scholar
Huang, W. M., Han, S. J., Xing, Z. F. et al. (2020b). Responses of leaf anatomy and CO2 concentrating mechanisms of the aquatic plant Ottelia cordata to variable CO2. Frontiers in Plant Science 11. 1261. https://doi.org/10.3389/fpls.2020.01261.CrossRefGoogle Scholar
Ito, Y., Tanaka, N., Barfod, A. S. et al. (2017). From terrestrial to aquatic habitats and back again: Molecular insights into the evolution and phylogeny of Callitriche (Plantaginaceae). Botanical Journal of the Linnean Society 184: 46–58.CrossRefGoogle Scholar
Iversen, L. L., Winkel, A., Baastrup-Spohr, L. et al. (2019). Catchment properties and the photosynthetic trait composition of freshwater plant communities. Science 366: 878–881.CrossRefGoogle ScholarPubMed
Keeley, J. E. (1981). Isoetes howelli – A submerged aquatic CAM plant. American Journal of Botany 68: 420–424.CrossRefGoogle Scholar
Keeley, J. E. (1998a). C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia 116: 85–97.CrossRefGoogle ScholarPubMed
Keeley, J. E. (1998b). CAM photosynthesis in submerged aquatic plants. Botanical Review 64: 121–175.CrossRefGoogle Scholar
Keeley, J. E. & Busch, G. (1984). Carbon assimilation characteristics of the aquatic CAM plant, Isoetes howellii. Plant Physiology 76: 525–530.CrossRefGoogle ScholarPubMed
Kirk, J. T. O. (2010). Light and Photosynthesis in Aquatic Environments, 3rd ed., Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Klančnik, K., Pančić, M. & Gaberščik, A. (2014). Leaf optical properties in amphibious plant species are affected by multiple leaf traits. Hydrobiologia 737: 121–130.CrossRefGoogle Scholar
Klavsen, S. K. & Maberly, S. C. (2009). Crassulacean acid metabolism contributes significantly to the in situ carbon budget in a population of the invasive aquatic macrophyte Crassula helmsii. Freshwater Biology 54: 105–118.CrossRefGoogle Scholar
Klavsen, S. K., Madsen, T. V. & Maberly, S. C. (2011). Crassulacean acid metabolism in the context of other carbon-concentrating mechanisms in freshwater plants: A review. Photosynthesis Research 109: 269–279.CrossRefGoogle ScholarPubMed
Koch, M., Bowes, G., Ross, C. et al. (2013). Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19: 103–132.CrossRefGoogle ScholarPubMed
Krause-Jensen, D. & Sand-Jensen, K. (1998). Light attenuation and photosynthesis of aquatic plant communities. Limnology and Oceanography 43: 396–407.CrossRefGoogle Scholar
Kuo, J. (2011). Cymodoceaceae. In Wilson, A. (ed.) Flora of Australia, Vol. 39, Australian Biological Resources Study, Canberra, pp. 120–134.Google Scholar
Kuo, J. (2020). Taxonomy of the genus Halophila thouars (Hydocharitaceae): A review. Plants 9: 1732.CrossRefGoogle ScholarPubMed
Lamb, J. B., van de Water, J. A. J. M., Bourne, D. G. et al. (2017). Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355: 731–733.CrossRefGoogle ScholarPubMed
Larkum, A. W. D., Davey, P. A., Kuo, J. et al. (2017). Carbon-concentrating mechanisms in seagrasses. Journal of Experimental Botany 68: 3773–3784.CrossRefGoogle ScholarPubMed
Larkum, A. W. D., Orth, R. J. & Duarte, C. M. (2006). Seagrasses: Biology, Ecology, and Conservation. Springer, Dordrecht, the Netherlands.Google Scholar
Les, D. H. (2015). Water from the rock: Ancient aquatic angiosperms flow from the fossil record. Proceedings of the National Academy of Sciences USA 112: 10825–10826.CrossRefGoogle ScholarPubMed
Les, D. H., Cleland, M. A. & Waycott, M. (1997). Phylogenetic studies in Alismatidae, II: Evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany 22: 443–463.CrossRefGoogle Scholar
Les, D. H. & Tippery, N. (2013). In time and with water … the systematics of alismatid monocotyledons. In: Wilkin, P. & Mayo, S. J., eds., Early Events in Monocot Evolution. Cambridge University Press, Cambridge, pp. 118–164.Google Scholar
Li, L., Lan, Z., Chen, J. & Song, Z. (2018). Allocation to clonal and sexual reproduction and its plasticity in Vallisneria spinulosa along a water-depth gradient. Ecosphere 9: e02070.CrossRefGoogle Scholar
Liu, Y., Johnson, M. G., Cox, C. J. et al. (2019). Resolution of the ordinal phylogeny of mosses using targeted exons from organellar and nuclear genomes. Nature Communications 10: 1485.CrossRefGoogle ScholarPubMed
Lloyd, J. & Farquhar, G. D. (1996). The CO2 dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with soil nutrient status. 1. General principles and forest ecosystems. Functional Ecology 10: 4–32.CrossRefGoogle Scholar
Lucas, W. J. (1982). Mechanism of acquisition of exogenous bicarbonate by internodal cells of Chara corallina. Planta 156: 181–192.CrossRefGoogle ScholarPubMed
Maberly, S. C. (1985). Photosynthesis by Fontinalis antipyretica 2. Assessment of environmental factors limiting photosynthesis and production. New Phytologist 100: 141–155.CrossRefGoogle Scholar
Maberly, S. C. (1993). Morphological and photosynthetic characteristics of Potamogeton obtusifolius from different depths. Journal of Aquatic Plant Management 31: 34–39.Google Scholar
Maberly, S. C. (2014). The fitness of the environments of air and water for photosynthesis, growth, reproduction and dispersal of photoautotrophs: An evolutionary and biogeochemical perspective. Aquatic Botany 118: 4–13.CrossRefGoogle Scholar
Maberly, S. C., Berthelot, S. A., Stott, A. W. et al. (2015). Adaptation by macrophytes to inorganic carbon down a river with naturally variable concentrations of CO2. Journal of Plant Physiology 172: 120–127.CrossRefGoogle Scholar
Maberly, S. C. & Gontero, B. (2017). Ecological imperatives for aquatic CO2-concentrating mechanisms. Journal of Experimental Botany 68: 3797–3814.CrossRefGoogle ScholarPubMed
Maberly, S. C. & Gontero, B. (2018). Trade-offs and synergies in the structural and functional characteristics of leaves photosynthesizing in aquatic environments. In: Adams III, W. W., Terashima, I. & Eaton-Rye, J. J. (eds.) The Leaf: A Platform for Performing Photosynthesis. Springer International Publishing, Cham, pp. 307–343.CrossRefGoogle Scholar
Maberly, S. C., Gontero, B., Puppo, C. et al. (2021). Inorganic carbon uptake in a freshwater diatom, Asterionella formosa (Bacillariophyceae): From ecology to genomics. Phycologia 60: 427–438.CrossRefGoogle Scholar
Maberly, S. C. & Madsen, T. V. (1998). Affinity for CO2 in relation to the ability of freshwater macrophytes to use HCO3−. Functional Ecology 12: 99–106.CrossRefGoogle Scholar
Maberly, S. C. & Spence, D. H. N. (1989). Photosynthesis and photorespiration in fresh-water organisms – amphibious plants. Aquatic Botany 34: 267–286.CrossRefGoogle Scholar
Madsen, T. V. (1987). The effect of different growth conditions on dark and light carbon assimilation in Littorella uniflora. Physiologia Plantarum 70: 183–188.CrossRefGoogle Scholar
Madsen, T. V. & Breinholt, M. (1995). Effects of air contact on growth, inorganic carbon sources and nitrogen uptake by an amphibious freshwater macrophyte. Plant Physiology 107: 149–154.CrossRefGoogle ScholarPubMed
Madsen, T. V., Olesen, B. & Bagger, J. (2002). Carbon acquisition and carbon dynamics by aquatic isoetids. Aquatic Botany 73: 351–371.CrossRefGoogle Scholar
Magnin, N. C., Cooley, B. A., Reiskind, J. B. et al. (1997). Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiology 115: 1681–1689.CrossRefGoogle ScholarPubMed
Mendonça, R., Müller, R. A., Clow, D. et al. (2017). Organic carbon burial in global lakes and reservoirs. Nature Communications 8: 1694.CrossRefGoogle ScholarPubMed
Morris, D. P., Zagarese, H., Williamson, C. E. et al. (1995). The attentuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography 40: 1381–1391.CrossRefGoogle Scholar
Morris, J. L., Puttick, M. N., Clark, J. W. et al. (2018). The timescale of early land plant evolution. Proceedings of the National Academy of Sciences USA 115: E2274–E2283.CrossRefGoogle ScholarPubMed
Murphy, K., Efremov, A., Davidson, T. A. et al. (2019). World distribution, diversity and endemism of aquatic macrophytes. Aquatic Botany 158: 103127.CrossRefGoogle Scholar
Olsen, J. L., Rouze, P., Verhelst, B. et al. (2016). The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530: 331–335.CrossRefGoogle ScholarPubMed
Papenbrock, J. (2012). Highlights in seagrasses’ phylogeny, physiology, and metabolism: What makes them special? ISRN Botany 2012: 103892.CrossRefGoogle Scholar
Pedersen, O. (1993). Long-distance water transport in aquatic plants. Plant Physiology 103: 1369–1375.CrossRefGoogle ScholarPubMed
Pedersen, O., Rich, S. M., Pulido, C. et al. (2011). Crassulacean acid metabolism enhances underwater photosynthesis and diminishes photorespiration in the aquatic plant Isoetes australis. New Phytologist 190: 332–339.CrossRefGoogle ScholarPubMed
Pedersen, O. & Sand-Jensen, K. (1992). Adaptations of submerged Lobelia dortmanna to aerial life form: Morphology, carbon sources and oxygen dynamics. Oikos 65: 89–96.CrossRefGoogle Scholar
PPG I. (2016). A community-derived classification for extant lycophytes and ferns: PPG I. Journal of Systematics and Evolution 54: 563–603.CrossRefGoogle Scholar
Prins, H. B. A. & Deguia, M. B. (1986). Carbon source of the water soldier, Stratiotes aloides L. Aquatic Botany 26: 225–234.CrossRefGoogle Scholar
Prins, H. B. A., & Elzenga, J. T. M. (1989). Bicarbonate utilization: Function and mechanism. Aquatic Botany, 34: 59–83.CrossRefGoogle Scholar
Prins, H. B. A., Snel, J. F. H., Helder, R. J. et al. (1980). Photosynthetic HCO3− utilization and OH– excretion in aquatic angiosperms: Light induced pH changes at the leaf surface. Plant Physiology 66: 818–822.CrossRefGoogle ScholarPubMed
Prins, H. B. A., Snel, J. F. H., Zanstra, P. E. et al. (1982). The mechanisms of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea: CO2 concentrations at the leaf surface. Plant Cell and Environment 5: 207–214.CrossRefGoogle Scholar
Raven, J. (2018). Blue carbon: Past, present and future, with emphasis on macroalgae. Biology Letters 14: 20180336.CrossRefGoogle ScholarPubMed
Raven, J. A. (2000). Land plant biochemistry. Philosophical Transactions of the Royal Society B 355: 833–846.CrossRefGoogle ScholarPubMed
Raven, J. A., Beardall, J. & Giordano, M. (2014). Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynthesis Research 121: 111–124.CrossRefGoogle ScholarPubMed
Reiskind, J. B., Madsen, T. V., Van Ginkel, L. C. et al. (1997). Evidence that inducible C4 type photosynthesis is a chloroplastic CO2 concentrating mechanism in Hydrilla, a submersed monocot. Plant Cell and Environment 20: 211–220.CrossRefGoogle Scholar
Riederer, M. & Schreiber, L. (2001). Protecting against water loss: Analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52: 2023–2032.CrossRefGoogle ScholarPubMed
Robe, W. E., & Griffiths, H. (2000). Physiological and photosynthetic plasticity in the amphibious, freshwater plant, Littorella uniflora, during the transition from aquatic to dry terrestrial environments. Plant Cell and Environment, 23: 1041–1054.CrossRefGoogle Scholar
Rubio, L., Garcia, D., Garcia-Sanchez, M. J. et al. (2017). Direct uptake of HCO3− in the marine angiosperm Posidonia oceanica (L.) Delile driven by a plasma membrane H+ economy. Plant Cell and Environment 40: 2820–2830.CrossRefGoogle ScholarPubMed
Sage, R. F., Monson, R. K., Ehleringer, J. R. et al. (2018). Some like it hot: The physiological ecology of C4 plant evolution. Oecologia 187: 941–966.CrossRefGoogle ScholarPubMed
Sage, R. F., Sage, T. L. & Kocacinar, F. (2012). Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63: 19–47.CrossRefGoogle ScholarPubMed
Salvucci, M. E. & Bowes, G. (1981). Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. Plant Physiology 67: 335–340.CrossRefGoogle ScholarPubMed
Sand-Jensen, K. (2003). Drag and reconfiguration of freshwater macrophytes. Freshwater Biology 48: 271–283.CrossRefGoogle Scholar
Sand-Jensen, K., Binzer, T. & Middelboe, A. L. (2007). Scaling of photosynthetic production of aquatic macrophytes – a review. Oikos 116: 280–294.Google Scholar
Scheffer, M., Hosper, S. H., Meijer, M. L. et al. (1993). Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275–279.CrossRefGoogle ScholarPubMed
Schuster, A.-C., Burghardt, M. & Riederer, M. (2017). The ecophysiology of leaf cuticular transpiration: Are cuticular water permeabilities adapted to ecological conditions? Journal of Experimental Botany 68: 5271–5279.CrossRefGoogle ScholarPubMed
Sculthorpe, C. D. (1967). The Biology of Aquatic Vascular Plants. Edward Arnold, London.Google Scholar
Shao, H., Gontero, B., Maberly, S. C. et al. (2017). Responses of Ottelia alismoides, an aquatic plant with three CCMs, to variable CO2 and light. Journal of Experimental Botany 68: 3985–3995.CrossRefGoogle ScholarPubMed
Silvera, K., Neubig, K. M., Whitten, W. M. et al. (2010). Evolution along the crassulacean acid metabolism continuum. Functional Plant Biology 37: 995–1010.CrossRefGoogle Scholar
Spence, D. H. N. & Chrystal, J. (1970). Photosynthesis and zonation of fresh-water macrophytes. 2. Adaptability of species of deep and shallow water. New Phytologist 69: 217–217.CrossRefGoogle Scholar
Steemann Nielsen, E. (1947). Photosynthesis of aquatic plants with special reference to the carbon sources. Dansk Botanisk Arkiv 12: 1–71.Google Scholar
Vadstrup, M. & Madsen, T. V. (1995). Growth limitation of submerged aquatic macrophytes by inorganic carbon. Freshwater Biology 34: 411–419.CrossRefGoogle Scholar
van Ginkel, L. C., Bowes, G., Reiskind, J. B. et al. (2001). A CO2-flux mechanism operating via pH-polarity in Hydrilla verticillata leaves with C3 and C4 photosynthesis. Photosynthesis Research 68: 81–88.CrossRefGoogle Scholar
Verpoorter, C., Kutser, T., Seekell, D. A. et al. (2014). A global inventory of lakes based on high-resolution satellite imagery. Geophysical Research Letters 41: 6396–6402.CrossRefGoogle Scholar
Vestergaard, O. & Sand-Jensen, K. (2000). Alkalinity and trophic state regulate aquatic plant distribution in Danish lakes. Aquatic Botany 67: 85–107.CrossRefGoogle Scholar
Voznesenskaya, E. V., Franceschi, V. R., Kiirats, O. et al. (2001). Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414: 543–546.CrossRefGoogle Scholar
Walker, N. A., Smith, F. A. & Cathers, I. R. (1980). Bicarbonate assimilation by fresh-water charophytes and higher plants: I. Membrane transport of bicarbonate ions is not proven. The Journal of Membrane Biology, 57: 51–58.CrossRefGoogle Scholar
Wang, M., Hu, C., Barnes, B. B. et al. (2019). The great Atlantic Sargassum belt. Science 365: 83–87.CrossRefGoogle ScholarPubMed
Westlake, D. F. (1963). Comparisons of plant productivity. Biological Reviews 38: 385–425.CrossRefGoogle Scholar
Wickett, N. J., Mirarab, S., Nguyen, N. et al. (2014). Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences USA 111: E4859–E4868.CrossRefGoogle ScholarPubMed
Winkel, A. & Borum, J. (2009). Use of sediment CO2 by submersed rooted plants. Annals of Botany 103: 1015–1023.CrossRefGoogle ScholarPubMed
Wium-Andersen, S. (1971). Photosynthetic uptake of free CO2 by roots of Lobelia dortmanna. Physiologia Plantarum 25: 245–248.CrossRefGoogle Scholar
Yin, L., Li, W., Madsen, T. V., Maberly, S. C. et al. (2017). Photosynthetic inorganic carbon acquisition in 30 freshwater macrophytes. Aquatic Botany 140: 48–54.CrossRefGoogle Scholar
Zhang, Y., Yin, L., Jiang, H.-S. et al. (2014). Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae). Photosynthesis Research 121: 285–297.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×