Abstract
Aquatic plants may face resource constraints or anthropogenic pollution, and effects might be heightened under multiple stress conditions. We investigated if arsenate effects on Myriophyllum spicatum L. would be stronger under CO2 limitation and low phosphorus availability. In a factorial design, we exposed sediment-grown plants to either CO2 (high carbon or HC) or bicarbonate (low carbon or LC) and four levels of arsenate. We observed strong effects of arsenate exposure on growth, biomass allocation (leaf, stem and root mass fractions), pigments and phenolic compounds. CO2 availability strongly affected the content in phenolic compounds and a few other response variables, yet overall effects were less pronounced than expected. Strong interactive effects of CO2 availability and arsenic concentration were only observed for carotenoids, the carotenoid/chlorophyll ratio and phenolic compounds in leaves. Only the carbon content declined with increasing arsenic concentration, otherwise leaf elemental content and stoichiometry were not affected by arsenic or CO2 availability, suggesting that plants strived to maintain leaf functions. The observed effects on biomass allocation and plant quality, specifically dry matter content and phenolic compound content of M. spicatum not only show direct changes in plant performance but suggest also indirect effects on ecological interactions such as competition or herbivory.
Similar content being viewed by others
References
AFNOR, 1990. Eaux-Méthodes d’Essais. Association Française de Normalisation (ed.). ISBN 2-12-179041-1.
Cedergreen, N., J. C. Streibig & N. H. Spliid, 2004. Sensitivity of aquatic plants to the herbicide metsulfuron-methyl. Ecotoxicology and Environmental Safety 57: 153–161.
Demars, B. O. L. & A. C. Edwards, 2007. Tissue nutrient concentrations in freshwater aquatic macrophytes: high inter-taxon differences and low phenotypic response to nutrient supply. Freshwater Biology 52: 2073–2086.
Dixon, R. A. & N. L. Pavia, 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085–1097.
Dushenko, W. T., D. A. Bright & K. J. Reimer, 1995. Arsenic bioaccumulation and toxicity in aquatic macrophytes exposed to gold-mine effluent: relationships with environmental partitioning, metal uptake and nutrients. Aquatic Botany 50: 141–158.
Elger, A. & N. J. Willby, 2003. Leaf dry matter content as an integrative expression of plant palatability: the case of freshwater macrophytes. Functional Ecology 17: 58–65.
Eusebio Malheiro, A. C., P. Jahns & A. Hussner, 2013. CO2 availability rather than light and temperature determines growth and phenotypical responses in submerged Myriophyllum aquaticum. Aquatic Botany 110: 31–37.
Finnegan, P. M. & W. Chen, 2012. Arsenic toxicity: the effects on plant metabolism. Frontiers in Physiology 3: 182.
Fornoff, F. & E. M. Gross, 2014. Induced defense mechanisms in an aquatic angiosperm to insect herbivory. Oecologia 175: 173–185.
Geng, C. N., Y. G. Zhu, W. J. Liu & S. E. Smith, 2005. Arsenate uptake and translocation in seedlings of two genotypes of rice is affected by external phosphate concentrations. Aquatic Botany 83: 321–331.
Grace, J. B. & R. G. Wetzel, 1978. The production biology of Eurasian watermilfoil (Myriophyllum spicatum L.): a review. Joural of Aquatic Plant Management 16: 1–11.
Gross, E. M., 2003. Differential response of tellimagrandin II and total bioactive hydrolysable tannins in an aquatic angiosperm to changes in light and nitrogen. Oikos 103: 497–504.
Gross, E. M. & E. S. Bakker, 2012. The role of plant secondary metabolites in freshwater macrophyte-herbivore interactions: limited or unexplored chemical defences? In Iason, G. R., M. Dicke & S. E. Hartley (eds.), The Integrative Role of Plant Secondary Metabolites in Ecological Systems. British Ecological Society/Cambridge University Press, Sussex: 154–169.
Guo, H. M., Z. N. Zhong, M. Lei, X. L. Xue, X. M. Wan, J. Y. Zhao & T. B. Chen, 2012. Arsenic uptake from arsenic-contaminated water using hyperaccumulator Pteris vittata L.: effect of chloride, bicarbonate, and arsenic species. Water Air and Soil Pollution 223: 4209–4220.
Güsewell, S. & M. Koerselman, 2002. Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology Evolution and Systematics 5: 37–61.
Harguinteguy, C. A., M. L. Pignata & A. Fernández-Cirelli, 2015. Nickel, lead and zinc accumulation and performance in relation to their use in phytoremediation of macrophytes Myriophyllum aquaticum and Egeria densa. Ecological Engineering 82: 512–516.
Hartley, S. E., C. G. Jones, G. C. Couper & T. H. Jones, 2000. Biosynthesis of plant phenolic compounds in elevated atmospheric CO2. Global Change Biology 6: 497–506.
Hussner, A. & P. Jahns, 2015. European native Myriophyllum spicatum showed a higher use capacity than alien invasive Myriophyllum heterophyllum. Hydrobiologia 746: 171–182.
Hussner, A., D. Hofstra, P. Jahns & J. Clayton, 2015. Response capacity to CO2 depletion rather than temperature and light effects explain the growth success of three alien Hydrocharitaceae compared with native Myriophyllum triphyllum in New Zealand. Aquatic Botany 120: 205–211.
Hussner, A., T. Mettler-Altmann, A. P. M. Weber & K. Sand-Jensen, 2016. Acclimation of photosynthesis to supersaturated CO2 in aquatic plant bicarbonate users. Freshwater Biology. doi:10.1111/fwb.12812.
Krayem, M., V. Deluchat, M. Rabiet, K. Cleries, J. F. Lenain, Z. Saad, V. Kazpard & P. Labrousse, 2016. Effect of arsenate As(V) on the biomarkers of Myriophyllum alterniflorum in oligotrophic and eutrophic conditions. Chemosphere 147: 131–137.
Lavid, N., A. Schwartz, O. Yarden & E. Tel-Or, 2001. The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta 212: 323–331.
Lê, S., J. Josse & F. Husson, 2008. FactoMineR: an R Package for Multivariate Analysis. Journal of Statistical Software. 25: 1–18.
Leao, G. A., J. A. de Oliveira, R. T. A. Felipe, F. S. Farnese & G. S. Gusman, 2014. Anthocyanins, thiols, and antioxidant scavenging enzymes are involved in Lemna gibba tolerance to arsenic. Journal of Plant Interactions 9: 143–151.
Leu, E., A. Krieger-Liszkay, C. Goussias & E. M. Gross, 2002. Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum L. inhibit photosystem II. Plant Physiology 130: 2011–2018.
Li, W., T. Cao, L. Y. Ni, G. R. Zhu, X. L. Zhang, H. Fu, X. Song & P. Xie, 2015. Size-dependent C, N and P stoichiometry of three submersed macrophytes along water depth gradients. Environmental Earth Sciences 74: 3733–3738.
Lichtenthaler, H. K. & C. Buschmann, 2001. Chlorophylls and Carotenoids: Measurement and Characterization by UV-VIS Spectroscopy Current Protocols in Food Analytical Chemistry. Wiley, New York.
Meybeck, M., 2004. The global change of continental aquatic systems: dominant impacts of human activities. Water Science and Technology 49: 73–83.
Mishra, S., H. J. Stark & H. Kupper, 2014. A different sequence of events than previously reported leads to arsenic-induced damage in Ceratophyllum demersum L. Metallomics 6: 444–454.
Mkandawire, M. & E. G. Dudel, 2012. Homeostatic regulation of elemental stoichiometry by Lemna gibba L. G3 when nutrient interact with toxic metals. Ecotoxicology 21: 456–464.
Murray, J. R. & W. P. Hackett, 1991. Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. Plant Physiology 97: 343–351.
Nuttens, A., S. Chatellier, S. Devin, C. Guignard, A. Lenouvel & E. M. Gross, 2016. Does nitrate co-pollution affect biological responses of an aquatic plant to two common herbicides? Aquatic Toxicology 177: 355–364.
OECD, 2014. TG 239: water-sediment Myriophyllum spicatum toxicity test. Test Guideline No. 239: 23.
Pérez-Harguindeguy, N., S. Díaz, E. Garnier, S. Lavorel, H. Poorter, P. Jaureguiberry, M. S. Bret-Harte, W. K. Cornwell, J. M. Craine, D. E. Gurvich, C. Urcelay, E. J. Veneklaas, P. B. Reich, L. Poorter, I. J. Wright, P. Ray, L. Enrico, J. G. Pausas, A. C. de Vos, N. Buchmann, G. Funes, F. Quétier, J. G. Hodgson, K. Thompson, H. D. Morgan, H. ter Steege, M. G. A. van der Heijden, L. Sack, B. Blonder, P. Poschlod, M. V. Vaieretti, G. Conti, A. C. Staver, S. Aquino & J. H. C. Cornelissen, 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167–234.
R Studio Team, 2015. RStudio: Integrated Development for R. RStudio Inc, Boston.
Rahman, M. A., H. Hasegawa & R. P. Lim, 2012. Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environmental Research 116: 118–135.
Reznik, H. & R. Neuhausel, 1959. Farblose Anthocyane bei submersen Wasserpflanzen. Zeitschrift für Botanik 47: 471–489.
Robinson, B., N. Kim, M. Marchetti, C. Moni, L. Schroeter, C. van den Dijssel, G. Milne & B. Clothier, 2006. Arsenic hyperaccumulation by aquatic macrophytes in the Taupo Volcanic Zone, New Zealand. Environmental and Experimental Botany 58: 206–215.
Sánchez-Viveros, G., R. Ferrera-Cerrato & A. Alarcón, 2011. Short-term effects of arsenate-induced toxicity on growth, chlorophyll and carotenoid contents, and total content of phenolic compounds of Azolla filiculoides. Water Air Soil Pollution 217: 455–462.
Segner, H., M. Schmitt-Jansen & S. Sabater, 2014. Assessing the impact of multiple stressors on aquatic biota: the receptor’s side matters. Environmental Science & Technology 48: 7690–7696.
Smart, R. M. & J. W. Barko, 1985. Laboratory culture of submersed freshwater macrophytes on natural sediments. Aquatic Botany 21: 251–263.
Smedley, P. L. & D. G. Kinniburgh, 2002. A review of the source, behaviour and distribution of arsenic in natural waters. Applied Geochemistry 17: 517–568.
Smith, C. S. & J. W. Barko, 1990. Ecology of Eurasian watermilfoil. Journal of Aquatic Plant Management 28: 55–64.
Taggart, M. A., R. Mateo, J. M. Charnock, F. Bahrami, A. J. Green & A. A. Meharg, 2009. Arsenic rich iron plaque on macrophyte roots – an ecotoxicological risk? Environmental Pollution 157: 946–954.
Tripathi, R. D., P. Tripathi, S. Dwivedi, A. Kumar, A. Mishra, P. S. Chauhan, G. J. Norton & C. S. Nautiyal, 2014. Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6: 1789–1800.
Waśkiewicz, A., M. Beszterda & P. Goliński, 2014. Nonenzymatic antioxidants in plants. In Ahmad, P. (ed), Oxidative Damage to Plants: Antioxidant Networks and Signaling. Academic Press, Amsterdam: 201–234.
Acknowledgments
We greatly appreciate the help of P. Rousselle with the C:N analyses, J.-F. Poinsaint with setting up the experimental infrastructure, S. Devin and L. Minguez for statistical advice. AH benefited from an invitation by the UFR SciFa, Univ Lorraine for a visit of 1 month. AN was funded by a PhD stipend from the MESR, Ministère de l’Enseignement Supérieur et de la Recherche, France. The experiment was possible due to funding for the project “PICAI—pollutant induced changes in allelochemical interactions” in the program ECODYN/EC2CO, INSU, CNRS to EMG and by support from the LTER–ZAM–Zone Atelier Moselle for AN, DP and EMG. We thank three anonymous reviewers and the editors of the special issue for constructive comments on prior versions of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: M. T. O’Hare, F. C. Aguiar, E. S. Bakker & K. A. Wood / Plants in Aquatic Systems – a 21st Century Perspective
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gross, E.M., Nuttens, A., Paroshin, D. et al. Sensitive response of sediment-grown Myriophyllum spicatum L. to arsenic pollution under different CO2 availability. Hydrobiologia 812, 177–191 (2018). https://doi.org/10.1007/s10750-016-2956-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-016-2956-7