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Biomechanical response of a submerged, rosette-forming macrophyte to wave action in a eutrophic lake on the Yungui Plateau, China

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Abstract

Few studies have focused on the biomechanical responses of submerged, rosette-forming macrophytes to wave action, water depth, or their co-occurrence in naturally eutrophic systems. The plant architecture, root anchorage strength-related traits, leaf morphology, and biomechanics of Vallisneria natans inhabiting a range of water depths were examined along three transects (T1, T2, and T3) in a eutrophic lake, Lake Erhai, in Yunnan Province, China. These transects were exposed to weak wave action and hyper-eutrophication (T1), moderate wave action and eutrophication (T2), or strong wave action and eutrophication (T3). The results showed that V. natans was mainly distributed at intermediate depths, with the widest colonization depth in T1. The values of plant architecture, root anchorage strength-related traits, leaf morphology, and biomechanics were generally highest in T3 and smallest in T2. Along the depth gradient, these values were generally highest at 3.5, 2.5, and 2.5 m for the plants growing in T1, T2, and T3, respectively. These findings suggest that V. natans adopts a “tolerance” strategy to cope with the effects of strong wave action in eutrophic habitats and an “avoidance” strategy when exposed to moderate wave action in eutrophic areas. Since the absence of an avoidance strategy increases the resistance to low-light stress at the expense of increased drag forces, there is a limit to the wave action that V. natans can withstand. This study indicates that biomechanics could be important when determining the distribution pattern of V. natans in Lake Erhai.

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References

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC 1268

    Google Scholar 

  • Bal KD, Bouma TJ, Buis K, Struyf E, Jonas S, Backx H, Meire P (2011) Trade-off between drag reduction and light interception of macrophytes: comparing five aquatic plants with contrasting morphology. Funct Ecol 25(6):1197–1205

    Google Scholar 

  • Boller ML, Carrington E (2006) The hydrodynamic effects of shape and size change during reconfiguration of a flexible macroalgae. J Exp Biol 209:1894–1903

    Google Scholar 

  • Brewer CA, Parker M (1990) Adaptations of macrophytes to life in moving water: upslope limits and mechanical properties of stems. Hydrobiologia 194:133–142

    Google Scholar 

  • Cao T, Ni LY, Xie P, Xu J, Zhang M (2011) Effects of moderate ammonium enrichment on three submersed macrophytes under contrasting light availability. Freshw Biol 56(8):1620–1629

    CAS  Google Scholar 

  • Capers RS, Selsky R, Bugbee GJ (2010) The relative importance of local conditions and regional processes in structuring aquatic plant communities. Freshw Biol 55(5):952–966

    Google Scholar 

  • Carrington E (1990) Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing. J Exp Mar Biol Ecol 139(3):185–200

    Google Scholar 

  • Carrington E (2013) Plant biomechanics: high-endurance algae. Nature 503(7476):345–346

    CAS  Google Scholar 

  • Chambers PA (1987a) Nearshore occurrence of submerged aquatic macrophytes in relation to wave action. Can J Fish Aquat Sci 44:1666–1669

    Google Scholar 

  • Chambers PA (1987b) Light and nutrients in control of aquatic plant community structure. II. In situ observations. J Ecol 75:621–628

    Google Scholar 

  • Chambers PA, Kalff J (1987) Light and nutrients in the control of aquatic plant community structure. 1. In situ experiments. J Ecol 75:611–619

    Google Scholar 

  • Chen JF, Cao T, Zhang XL, Xi YL, Ni LY, Jeppesen E (2016) Differential photosynthetic and morphological adaptations to low light affect depth distribution of two submersed macrophytes in lakes. Sci Rep 6:1–9

    Google Scholar 

  • Chu ZS, Chen SQ, Wang CC, Ye BB, Pang Y (2014) Temporal-spatial distribution of submerged macrophyte residues transported by wind wave in Lake Erhai. Res Environ Sci 27(1):6–11 (in Chinese)

    Google Scholar 

  • Crook MJ, Ennos AR (1996) Mechanical differences between freestanding and supported wheat plants Triticum aestivum L. Ann Bot 77:197–202

    Google Scholar 

  • Dawson FH, Robinson WN (1984) Submersed macrophytes and the hydraulic roughness of a lowland chalkstream. Verh int Ver Limnol 22:1944–1948

    Google Scholar 

  • de los Santos CB, Brun FG, Bouma TJ, Vergara JJ, Pérez-LLoréns JL (2016) Acclimation of seagrass Zostera noltii to co-occurring hydrodynamic and light stresses. Mar Ecol Prog Ser 398:127–135

    Google Scholar 

  • Denny MW (1988) Biology and the mechanics of the wave-swept environment. Princeton University Press, Princeton

    Google Scholar 

  • Doyle RD (2001) Effects of waves on the early growth of Vallisneria americana. Freshw Biol 46(3):389–397

    Google Scholar 

  • Eaton AD, Clesceri LS, Greenberg AE, Branson MAH (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Escribano MR, Santalla M, de Ron AM (1997) Genetic diversity in pod and seed quality traits of common bean populations from northwestern Spain. Euphytica 93:71–81

    Google Scholar 

  • Fu H, Yuan GX, Cao T, Ni LY, Zhang M, Wang SR (2012) An alternative mechanism for shade adaptation: implication of allometric responses of three submersed macrophytes to water depth. Ecol Res 27:1087–1094

    Google Scholar 

  • Fu H, Yuan GX, Zhong JY, Cao T, Ni LY, Xie P (2013) Environmental and ontogenetic effects on intraspecific trait variation of a macrophyte species across five ecological scales. PLoS One 8(4):e62794–e62794

    CAS  Google Scholar 

  • Fu H, Zhong JY, Yuan GX, Ni LY, Xie P, Cao T (2014) Functional traits composition predict macrophytes community productivity along a water depth gradient in a freshwater lake. Ecol Evol 4(9):1516–1523

    Google Scholar 

  • Gaylord B, Hale BB, Denny MW (2001) Consequences of transient fluid forces for compliant benthic organisms. J Exp Biol 204:1347–1360

    CAS  Google Scholar 

  • Goodman AM, Ennos AR (1996) A comparative study of the response of the roots and shoots of sunflower and maize to mechanical stimulation. J Exp Bot 47:1499–1507

    CAS  Google Scholar 

  • Hamann E, Puijalon S (2013) Biomechanical responses of aquatic plants to aerial conditions. Ann Bot 112:1869–1878

    Google Scholar 

  • Handley RJ, Davy AJ (2002) Seedling root establishment may limit Najas marina L. to sediments of low cohesive strength. Aquat Bot 73:129–136

    Google Scholar 

  • Haslam SM (2006) River plants. The macrophytic vegetation of watercourses. Forrest Text, Cardigan

    Google Scholar 

  • He L (2015) Regulating factors for growth and distribution of submerged macrophytes in lakes—eutrophication, warming and lake morphometry. PhD Thesis, Institute of Hydrobiology, The Chinese Academy of Sciences, P.R. China (in Chinese)

  • Hu X, Jin X, Du B, Zhu J (2005) Submerged macrophyte of lake Erhai and it’s dynamic change. Res Environ Sci 18:1–5 (in Chinese)

    Google Scholar 

  • Huang X, Shen N, Guan X, Xu X, Kong F, Liu C, Yu D (2018) Root morphological and structural comparisons of introduced and native aquatic plant species in multiple substrates. Aquat Ecol 52(1):65–76

    Google Scholar 

  • IPCC (2014) Summary for policymakers. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: Impacts, adaptation, and vulnerability. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1–32

    Google Scholar 

  • Istvánovics V, Honti M, Kovács Á, Osztoics A (2008) Distribution of submerged macrophytes along environmental gradients in large, shallow Lake Balaton (Hungary). Aquat Bot 88:317–330

    Google Scholar 

  • Jin G (1995) Preliminary observation on the recovery and growth of Vallisneria spiralis after grass carp (Ctenopharyngodon idellus) grazing. Resources, environment and fishery ecological management of macrophytic lakes. Science Press, Beijing, pp 227–235

    Google Scholar 

  • Kalra YP, Maynard DG (1991) Methods manual for forest soil and plant analysis. Forestry Canada, Northwest Region, Northern Forestry Centre NOR-X-319

  • Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems, 2. Cambridge University Press, New York, p 509

    Google Scholar 

  • Koehl MAR (1984) How do benthic organisms withstand moving water? Am Zool 24:57–70

    Google Scholar 

  • Koehl MAR, Wainwright SA (1973) Biomechanics. In: Littler MM, Littler DS (eds) Handbook of phycological methods, vol 4. Cambridge University Press, Cambridge, pp 291–315

    Google Scholar 

  • Kopp BS (1999) Effects of nitrate fertilization and shading on physiological and biomechanical properties of eelgrass (Zostera marina L.). PhD Thesis, University of Rhode Island, Rhode Island

  • Lamberti-Raverot B, Puijalon S (2012) Nutrient enrichment affects the mechanical resistance of aquatic plants. J Exp Bot 63:6115–6123. https://doi.org/10.1093/jxb/ers268

    CAS  Google Scholar 

  • La Nafie YA, de los Santos CB, Brun FG, van Katwijk MM, Bouma TJ (2012) Waves and high nutrient loads jointly decrease survival and separately affect morphological and biomechanical properties in the seagrass Zostera noltii. Limnol Oceanogr 57(6):1664–1672

    Google Scholar 

  • La Nafie YA, Carmen B, Brun FG, Mashoreng S, van Katwijk MM, Bouma TJ (2013) Biomechanical response of two fast-growing tropical seagrass species subjected to in situ shading and sediment fertilization. J Exp Mar Biol Ecol 446:186–193

    Google Scholar 

  • Lane RH (1936) The inhibition of roots by growth hormone. Am J Bot 23:532–535

    CAS  Google Scholar 

  • Li L, Bonser SP, Lan ZC, Xu LG, Chen JK, Song ZP (2017) Water depth affects reproductive allocation and reproductive allometry in the submerged macrophyte Vallisneria natans. Sci Rep 7(1):16842

    Google Scholar 

  • Liu H, Feng J, Sun J, Wang L, Xu A (2015) Eddy covariance measurements of water vapor and CO2 fluxes above the Erhai Lake. Sci China Earth Sci 58(3):317–328

    CAS  Google Scholar 

  • Lubsch A, Timmermans K (2017) Texture analysis of Laminaria digitata (Phaeophyceae) thallus reveals trade-off between tissue tensile strength and toughness along lamina. Bot Mar 60(2):229–237

    Google Scholar 

  • Mason R (1967) The species of Ruppia in New Zealand. New Zeal J Bot 5(4):519–531

    Google Scholar 

  • Miler O, Albayrak I, Nikora V, O’Hare M (2012) Biomechanical properties of aquatic plants and their effects on plant-flow interactions in streams and rivers. Aquat Sci 74:31–44

    Google Scholar 

  • Miler O, Albayrak I, Nikora V, O'Hare M (2014) Biomechanical properties and morphological characteristics of lake and river plants: implications for adaptations to flow conditions. Aquat Sci 76(4):465–481

    Google Scholar 

  • Mullarney JC, Pilditch CA (2017) The differential response of kelp to swell and infragravity wave motion. Limnol Oceanogr 62(6):2524–2537

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Google Scholar 

  • OECD (Organization for Economic Cooperation and Development) (1982) Eutrophication of waters: monitoring assessment and control. Final report. OECD Cooperative Programme on Monitoring of Inland Waters (Eutrophication Control). Environment Directorate, OECD, Paris, p 154

    Google Scholar 

  • Patterson MR, Harwell MC, Orth LM, Orth RJ (2001) Biomechanical properties of the reproductive shoots of eelgrass. Aquat Bot 69:27–40

    Google Scholar 

  • Paul M, Henry PY, Thomas RE (2014) Geometrical and mechanical properties of four species of northern European brown macroalgae. Coast Eng 84:73–80

    Google Scholar 

  • Pratt MC, Johnson AS (2002) Strength, drag, and dislodgment of two competing intertidal algae from two wave exposures and four seasons. J Exp Mar Biol Ecol 272:71–101

    Google Scholar 

  • Puijalon S, Bornette G, Sagnes P (2005) Adaptations to increasing hydraulic stress: morphology, hydrodynamics and fitness of two higher aquatic plant species. J Exp Bot 56:777–786

    CAS  Google Scholar 

  • Puijalon S, Léna JP, Rivière N, Champagne JY, Rostan JC, Bornette G (2008) Phenotypic plasticity in response to mechanical stress: hydrodynamic performance and fitness of four aquatic plant species. New Phytol 177:907–917

    Google Scholar 

  • Puijalon S, Bouma TJ, Douady CJ, Groenendael J, Anten NPR, Martel E, Bornette G (2011) Plant resistance to mechanical stress: evidence of an avoidance–tolerance trade-off. New Phytol 191:1141–1149

    CAS  Google Scholar 

  • Riis T, Hawes I (2003) Effect of wave exposure on vegetation abundance, richness and depth distribution of shallow water plants in a New Zealand lake. Freshw Biol 48(1):75–87

    Google Scholar 

  • Robionek A, Banaś K, Chmara R, Szmeja J (2015) The avoidance strategy of environmental constraints by an aquatic plant Potamogeton alpinus in running waters. Ecol Evol 5(16):3327–3337

    Google Scholar 

  • Ross JK (1981) The radiation regime and the architecture of plant stands. Junk W. Pubs., The Hague

    Google Scholar 

  • Sand-Jensen K (2003) Drag and reconfiguration of freshwater macrophytes. Freshw Biol 48(2):271–283

    Google Scholar 

  • Schutten J, Davy AJ (2000) Predicting hydraulic forces on submerged macrophytes from current velocity, biomass and morphology. Oecologia 123:445–452

    CAS  Google Scholar 

  • Schutten J, Dainty J, Davy AJ (2004) Wave-induced hydraulic forces on submersed aquatic plants in shallow lakes. Ann Bot 93:333–341

    CAS  Google Scholar 

  • Schutten J, Dainty J, Davy AJ (2005) Root anchorage and its significance for submersed plants in shallow lakes. J Ecol 93:556–571

    Google Scholar 

  • Soissons LM, Van Katwijk MM, Peralta G et al (2018) Seasonal and latitudinal variation in seagrass mechanical traits across Europe: the influence of local nutrient status and morphometric plasticity. Limnol Oceanogr 63(1):37–46

    CAS  Google Scholar 

  • Starko S, Barry ZC, Martone PT (2015) Biomechanical consequences of branching in flexible wave-swept macroalgae. New Phytol 206(1):133–140

    Google Scholar 

  • Stewart RM, McFarland DG, Ward DL, Martin SK, Barko JW (1997) Flume study investigation of navigation-generated waves on submersed aquatic macrophytes in the Upper Mississippi River. Upper Mississippi River – Illinois Waterway System Navigation Study. ENV Report 1, September 1997. 62 pp

  • Tucker GF, Emmingham WH (1977) Morphological changes in leaves of residual western hemlock after clear and shelterwood cutting. For Sci 23(2):195–203

    Google Scholar 

  • Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

    Google Scholar 

  • Usherwood JR, Ennos AR, Ball DJ (1997) Mechanical and anatomical adaptations in terrestrial and aquatic buttercups to their respective environments. J Exp Bot 312:1469–1475

    Google Scholar 

  • Van Zuidam BG, Peeters ET (2015) Wave forces limit the establishment of submerged macrophytes in large shallow lakes. Limnol Oceanogr 60(5):1536–1549

    Google Scholar 

  • Verduin JJ, Backhaus JO (2000) Dynamics of plant–flow interactions for the seagrass Amphibolis antarctica: field observations and model simulations. Estuar Coast Shelf Sci 50(2):185–204

    Google Scholar 

  • Vogel S (1989) Drag and reconfiguration of broad leaves in high winds. J Exp Bot 40:941–948

    Google Scholar 

  • Vogel S (1994) Life in moving fluids: the physical biology of flow. Princeton University Press, Princeton

    Google Scholar 

  • Wang R, Dearin JA, Langdon PG, Zhang E, Yang X, Dakos V, Scheffer M (2012) Flickering gives early warning signals of a critical transition to a eutrophic lake state. Nature 492:419–422

    Google Scholar 

  • Wei ZH, Yang ZX, Tang XF, Lv XJ, Zhu J, Dou JS, Yang SK, Liang M (2013) Three-dimensional modeling and characteristics of hydrodynamic processes in Erhai Lake. J Kunming Uni Sci Tech 38(1):85–95 (in Chinese)

    CAS  Google Scholar 

  • Wu Q, Wang Y (1998) On the succession of aquatic communities in Erhai Lake. J Lake Sci 11:267–273 (in Chinese)

    Google Scholar 

  • Xie Y, An S, Wu B (2005) Resource allocation in the submerged plant Vallisneria natans related to sediment type, rather than water–column nutrients. Freshw Biol 50(3):391–402

    Google Scholar 

  • Xu AL, Zhao XH, Fu ZJ, Liu JS, Sun JH (2011) Comparison of meteorological elements over water and land surfaces in the Erhai Lake basin. Trans Atmos Sci 34(2):225–231 (in Chinese)

    Google Scholar 

  • Xu LJ, Liu HZ, Cao J (2014) Numerical simulation of local circulation over the Cangshan Mountain−Erhai Lake area in Dali, Southwest China. Chin J Atmos Sci 38(6):1198–1210 (in Chinese)

    Google Scholar 

  • Xu W, Hu W, Deng J, Zhu J, Zhou N, Liu X (2016) Impacts of water depth and substrate type on Vallisneria natans at wave-exposed and sheltered sites in a eutrophic large lake. Ecol Eng 97:344–354

    Google Scholar 

  • Ye BB, Chu ZS, Wu AP, Hou ZY, Wang SR (2018) Optimum water depth ranges of dominant submersed macrophytes in a natural freshwater lake. PLoS One 13(3):e0193176

    Google Scholar 

  • Young IR, Zieger S, Babanin AV (2011) Global trends in wind speed and wave height. Science 332:451–455

    CAS  Google Scholar 

  • Zhang Y, Qiu LW, Yang BL, Li J, Wang YL (2016) Effects of water level fluctuation on sedimentary characteristics and reservoir architecture of a lake, river dominated delta. J Cent South Univ 23:2958–2971

    Google Scholar 

  • Zhu GR, Li W, Zhang M, Ni LY, Wang SR (2012a) Adaptation of submerged macrophytes to both water depth and flood intensity as revealed by their mechanical resistance. Hydrobiologia 696(1):77–93

    Google Scholar 

  • Zhu GR, Zhang M, Cao T, Ni LY, Zhong AW, Fu H (2012b) Effects of sediment type on stem mechanical properties of the submerged macrophyte Hydrilla verticillata (L.f.) Royle. Fresenius Environ Bull 21:468–474

    CAS  Google Scholar 

  • Zhu GR, Cao T, Zhang M, Ni LY, Zhang XL (2014) Fertile sediment and ammonium enrichment decrease the growth and biomechanical strength of submersed macrophyte Myriophyllum spicatum in an experiment. Hydrobiologia 727:109–120

    Google Scholar 

  • Zhu GR, Zhang M, Cao T, Ni LY (2015) Associations between the morphology and biomechanical properties of submerged macrophytes implications for its survival and distribution in Lake Erhai. Environ Earth Sci 74(5):3907–3916

    CAS  Google Scholar 

  • Zhu ZJ, Song SY, Yan YE, Li PS, Jeelani N, Wang P, An SQ, Leng X (2017) Combined effects of light reduction and ammonia nitrogen enrichment on the submerged macrophyte Vallisneria natans. Mar Freshw Res 69:764. https://doi.org/10.1071/MF17146

    Article  CAS  Google Scholar 

  • Zhu GR, Yuan CB, Di GL, Zhang M, Ni LY, Cao T, Fang RT, Wu G (2018) Morphological and biomechanical response to eutrophication and hydrodynamic stresses. Sci Total Environ 622:421–435

    Google Scholar 

  • Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Can J Bot 56:2286–2295

    Google Scholar 

  • Kopp BS1999

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Acknowledgements

We are grateful to the anonymous reviewers for their helpful remarks on the manuscript. We thank Mr. H Fu, W Zhang, X Tang, CH Cui, and several others for their help with the field sampling and in the laboratory. We also thank Alison Beamish of the University of British Columbia, as well as Alexander Ebbing and Jaco de Smit of the Royal Netherlands Institute for Sea Research, for the assistance with the English language and grammar and general presentation of the manuscript.

Funding

This work was co-supported by the National High Technology Research and Development Program of China (Grant No. 2012ZX07105-004), the National Natural Science Foundation of China (Grant No. 31400402), a Brainstorm Project on Social Development by the Department of Science and Technology of Henan Province (142102310476), and the China Scholarship Council and Research Fund for the Doctoral Program of Higher Education of China (qd13049).

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Zhu, G., Di, G., Zhang, M. et al. Biomechanical response of a submerged, rosette-forming macrophyte to wave action in a eutrophic lake on the Yungui Plateau, China. Environ Sci Pollut Res 25, 34027–34045 (2018). https://doi.org/10.1007/s11356-018-3047-2

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