Are soil resources a limiting factor of alpine plants’ seed reproduction?

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

Mineral nutrients are often regarded as important factors limiting the fitness of plant species through their seed production. However, numerous studies investigating the effects of soil nutrient enrichment in seed production have contradictory results and usually are short-term. In the present study, we aimed to investigate the response of the reproductive traits (number of generative shoots, NGS) of alpine plants to long-term (26 years) nutrient addition and to assess the applicability of the Liebig’s law to a natural plant community. We added individual soil resources (N, P, Ca, water) and their combination (NP) in alpine lichen heath (ALH) to remove potential limitation of generative shoot production. Studied nutrients did not limit NGS of ALH plants in general: the sum of generative shoots of all species from each variant did not increase during the experiment. In contrast, P addition and irrigation decreased it. Species diversity of generative shoots decreased after long-term N, P, and NP additions. Calcium did not decrease NGS in any studied species, but several species increased NGS after liming. The response of individual species was individual. The NGS of Trifolium polyphyllum (a non-nitrogen-fixing legume) increased in the N treatment, in contrary to the typical response of legumes to nitrogen fertilizers. The response of about half of the ALH species confirm the Liebig’s law (positive response to only one of the separately applied nutrients); while the remaining species did not show a positive response to the addition of individual nutrients. Only Carex umbrosa responded positively to both nitrogen and phosphorus applications.

Palavras-chave

-

Sobre autores

Yu. Sofronov

Lomonosov Moscow State University; Institute of Atmospheric Physics, RAS

Autor responsável pela correspondência
Email: sofronovyuriy163@gmail.com

Biological Faculty, Department of Plants Ecology and Geography; Laboratory of Mathematical Ecology

Rússia, Leninskie Gory, 1, Bld. 12, Moscow, 119234; Pyzhevsky Lane, 3, Moscow, 119017

D. Khomyakov

Lomonosov Moscow State University

Email: sofronovyuriy163@gmail.com

Biological Faculty, Department of Plants Ecology and Geography

Rússia, Leninskie Gory, 1, Bld. 12, Moscow, 119234

T. Elumeeva

Lomonosov Moscow State University

Email: sofronovyuriy163@gmail.com

Biological Faculty, Department of Plants Ecology and Geography

Rússia, Leninskie Gory, 1, Bld. 12, Moscow, 119234

V. Makhantseva

Institute of Physical-Chemical and Biological Problems of Soil Science, RAS

Email: sofronovyuriy163@gmail.com
Rússia, Institutskaya, 2, Pushchino, Moscow Region, 142290

A. Akhmetzhanova

Lomonosov Moscow State University

Email: sofronovyuriy163@gmail.com

Biological Faculty, Department of Plants Ecology and Geography

Rússia, Leninskie Gory, 1, Bld. 12, Moscow, 119234

V. Onipchenko

Lomonosov Moscow State University; Teberda State Biosphere Reserve; Aliyev Karachay-Cherkess State University

Email: sofronovyuriy163@gmail.com

Biological Faculty, Department of Plants Ecology and Geography

Rússia, Leninskie Gory, 1, Bld. 12, Moscow, 119234; Baduksky Lane, 1, Teberda, Karachay-Cherkess Republic, 369210; Lenin str., 29, Karachayevsk, Karachay-Cherkess Republic, 369202

Bibliografia

  1. Гришина Л.А., Онипченко В.Г., Макаров М.И., 1986. Состав и структура биогеоценозов альпийских пустошей. М.: Изд-во МГУ. С. 24–37.
  2. Гришина Л.А., Онипченко В.Г., Макаров М.И., Ванясин В.А., 1993. Изменения свойств горно-луговых альпийских почв северо-западного Кавказа в различных экологических условиях // Почвоведение. № 4. С. 5–13.
  3. Егоров А.В., Онипченко В.Г., Текеев Д.К., 2012. Экологические характеристики высокогорных растений Тебердинского заповедника. М.: МИЛ. 255 с.
  4. Лавренов Н.Г., Заузанова Л.Д., Онипченко В.Г., 2017. Параметры семенного размножения альпийских растений в зависимости от обогащения почвы // Экология. № 6. С. 454–460.
  5. Онипченко В.Г., 2014. Функциональная фитоценология. Синэкология растений. Изд. 2-е. М.: КРАСАНД. 576 с.
  6. Онипченко В.Г., Зернов А.С., 2022. Сосудистые растения Тебердинского национального парка / Флора и фауна заповедников. Вып. 99Б. М.: Изд. Комиссии РАН по сохранению биологического разнообразия и ИПЭЭ РАН. 177 с.
  7. Работнов Т.А., 1985. Экология луговых трав. М.: Изд-во МГУ. 176 с.
  8. Шидаков И.И., Текеев Д.К., 2009. Эколого-морфологические особенности листьев альпийских растений Тебердинского заповедника Башкирский государственный университет. Кисловодск: МИЛ. 104 с.
  9. Ariina M.S., 2021. Properties of soil in relation to altitude // Just Agric. V. 1. № 12. Art. 035.
  10. Barrow N.J., Hartemink A.E., 2023. The effects of pH on nutrient availability depend on both soils and plants // Plant Soil. V. 487. № 1–2. P. 21–37.
  11. Bassin S., Schalajda J., Vogel A., Suter M., 2012. Different types of sub‐alpine grassland respond similarly to elevated nitrogen deposition in terms of productivity and sedge abundance // J. Veg. Sci. V. 23. № 6. Р. 1024–1034.
  12. Bassin S., Volk M., Suter M., Buchmann N., Fuhrer J., 2007. Nitrogen deposition but not ozone affects productivity and community composition of subalpine grassland after 3 yr of treatment // New Phytol. V. 175. № 3. Р. 523–534.
  13. Bassin S., Werner R.A., Sörgel K., Volk M., Buchmann N., Fuhrer J., 2009. Effects of combined ozone and nitrogen deposition on the in situ properties of eleven key plant species of a subalpine pasture // Oecologia. V. 158. № 4. Р. 747–756.
  14. Berendse F., Geerts R.H.E.M., Elberse W.T., Bezemer T.M., Goedhart P.W., et al., 2021. A matter of time: Recovery of plant species diversity in wild plant communities at declining nitrogen deposition // Divers. Distrib. V. 27. № 7. Р. 1180–1193.
  15. Blanke V., Bassin S., Volk M., Fuhrer J., 2012. Nitrogen deposition effects on subalpine grassland: The role of nutrient limitations and changes in mycorrhizal abundance // Acta Oecologica. V. 45. Р. 57–65.
  16. Bowman W.D., Ayyad A., Bueno De Mesquita C.P., Fierer N., Potter T.S., Sternagel S., 2018. Limited ecosystem recovery from simulated chronic nitrogen deposition // Ecol. Appl. V. 28. № 7. Р. 1762–1772.
  17. Bowman W.D., Bahn L., Damm M., 2003. Alpine landscape variation in foliar nitrogen and phosphorus concentrations and the relation to soil nitrogen and phosphorus availability // Arctic Antarctic Alpine Res. V. 35. № 2. Р. 144–149.
  18. Britton A.J., Mitchell R.J., Fisher J.M., Riach D.J., Taylor A.F.S., 2018. Nitrogen deposition drives loss of moss cover in alpine moss–sedge heath via lowered C : N ratio and accelerated decomposition // New Phytol. V. 218. № 2. Р. 470–478.
  19. Burkle L.A., Irwin R.E., 2010. Beyond biomass: Measuring the effects of community‐level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction // J. Ecol. V. 98. № 3. Р. 705–717.
  20. Chen Y., Liu X., Hou Y., Zhou S., Zhu B., 2021. Particulate organic carbon is more vulnerable to nitrogen addition than mineral-associated organic carbon in soil of an alpine meadow // Plant Soil. V. 458. № 1–2. Р. 93–103.
  21. Darcy J.L., Schmidt S.K., Knelman J.E., Cleveland C.C., Castle S.C., Nemergut D.R., 2018. Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat // Sci. Adv. V. 4. № 5. Art. eaaq0942.
  22. Dolédec S., Chessel D., Ter Braak C.J.F., Champely S., 1996. Matching species traits to environmental variables: A new three-table ordination method // Environ. Ecol. Stat. V. 3. № 2. Р. 143–166.
  23. Eckert C.G., Barrett S.C.H., 1993. Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus (Lythraceae) // Am. J. Bot. V. 80. № 10. Р. 1175–1182.
  24. Elumeeva T.G., Onipchenko V.G., Egorov A.V., Khubiev A.B., Tekeev D.K., et al., 2013. Long-term vegetation dynamic in the Northwestern Caucasus: Which communities are more affected by upward shifts of plant species? // Alpine Вot. V. 123. № 2. Р. 77–85.
  25. Eskelinen A., Kaarlejärvi E., Olofsson J., 2017. Herbivory and nutrient limitation protect warming tundra from lowland species invasion and diversity loss // Global Change Biol. V. 23. № 1. Р. 245–255.
  26. Fisher R.A., 1930. The Genetical Theory of Natural Selection. Oxford: At The Clarendon Press. 308 p.
  27. Fortier R., Wright S.J., 2021. Nutrient limitation of plant reproduction in a tropical moist forest // Ecology. V. 102. № 10. Art. e03469.
  28. Friedman J., Rubin M.J., 2015. All in good time: Understanding annual and perennial strategies in plants // Am. J. Bot. V. 102. № 4. P. 497–499.
  29. Gigon A., 1987. A Hierarchic Approach in Causal Ecosystem Analysis The Calcifuge-Calcicole Problem in Alpine Grasslands // Potentials and Limitations of Ecosystem Analysis. V. 61 / Eds Schulze E.-D., Zwolfer H. Berlin: Springer. P. 228–244.
  30. Grime J.P., 2006. Plant Strategies, Vegetation Processes, and Ecosystem Properties. Hoboken: John Wiley & Sons. 464 p.
  31. Güsewell S., 2004. N : P ratios in terrestrial plants: variation and functional significance // New Phytol. V. 164. № 2. P. 243–266.
  32. Hamilton L.S., McMillan L., 2004. Guidelines for Planning and Managing Mountain Protected Areas. Gland; Cambridge: IUCN. 83 p.
  33. Harpole W.S., Ngai J.T., Cleland E.E., Seabloom E.W., Borer E.T., et al., 2011. Nutrient co-limitation of primary producer communities // Ecol. Lett. V. 14. № 9. Р. 852–862.
  34. Harpole W.S., Sullivan L.L., Lind E.M., Firn J., Adler P.B., et al., 2017. Out of the shadows: Multiple nutrient limitations drive relationships among biomass, light and plant diversity // Funct. Ecol. V. 31. № 9. P. 1839–1846.
  35. Harpole W.S., Tilman D., 2007. Grassland species loss resulting from reduced niche dimension // Nature. V. 446. № 7137. P. 791–793.
  36. Haugwitz M.S., Michelsen A., 2011. Long-term addition of fertilizer, labile carbon, and fungicide alters the biomass of plant functional groups in a subarctic-alpine community // Plant Ecol. V. 212. № 4. Р. 715–726.
  37. Heer C., Körner C., 2002. High elevation pioneer plants are sensitive to mineral nutrient addition // Basic Appl. Ecol. V. 3. № 1. P. 39–47.
  38. Holzmann H.-P., Haselwandter K., 1988. Contribution of nitrogen fixation to nitrogen nutrition in an alpine sedge community (Caricetum curvulae) // Oecologia. V. 76. № 2. P. 298–302.
  39. Hooper D.U., Johnson L., 1999. Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation // Biogeochemistry. V. 46. № 1–3. P. 247–293.
  40. Kenk G., Fischer H., 1988. Evidence from nitrogen fertilisation in the forests of Germany // Environ. Pollut. V. 54. № 3–4. P. 199–218.
  41. Körner C., 1984. Auswirkungen von Mineraldünger auf alpine Zwergsträucher // Verhandlungen der Gesellschaft für Ökologie. V. 12. P. 123–136.
  42. Körner C., 2003. Alpine Plant Life. 2nd ed. Berlin: Springer. 344 p.
  43. Kumar S., Suyal D.C., Yadav A., Shouche Y., Goel R., 2019. Microbial diversity and soil physiochemical characteristic of higher altitude // PLoS One. V. 14. № 3. Art. e0213844.
  44. Lafrenière M.J., Sinclair K.E., 2011. Snowpack and precipitation chemistry at a high altitude site in the Canadian Rocky Mountains // J. Hydrol. V. 409. № 3. P. 737–748.
  45. LeBauer D.S., Treseder K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed // Ecology. V. 89. № 2. P. 371–379.
  46. Lekberg Y., Arnillas C.A., Borer E.T., Bullington L.S., Fierer N., et al., 2021. Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils // Nat. Commun. V. 12. № 1. P. 34–84.
  47. Li Z., Wu J., Han Q., Nie K., Xie J., et al., 2021. Nitrogen and litter addition decreased sexual reproduction and increased clonal propagation in grasslands // Oecologia. V. 195. № 1. P. 131–144.
  48. Liebig J., von, 1842. Animal Chemistry, or Organic Chemistry in its Application to Physiology and Pathology. N.-Y.: Johnson Reprint Corporation. 347 p.
  49. Lin C., Wang Y., Liu M., Li Q., Xiao W., Song X., 2020. Effects of nitrogen deposition and phosphorus addition on arbuscular mycorrhizal fungi of Chinese fir (Cunninghamia lanceolata) // Sci. Rep. V. 10. Art. 12260.
  50. Liu X., Lu Y., Zhang Z., Zhou S., 2020. Foliar fungal diseases respond differently to nitrogen and phosphorus additions in Tibetan alpine meadows // Ecol. Res. V. 35. № 1. P. 162–169.
  51. Ma B., Zhou X., Zhang Q., Qin M., Hu L., et al., 2019. How do soil micro‐organisms respond to N, P and NP additions? Application of the ecological framework of (co‐)limitation by multiple resources // J. Ecol. V. 107. № 5. P. 2329–2345.
  52. Mittelbach G.G., Steiner C.F., Scheiner S.M., Gross K.L., Reynolds H.L., et al., 2001. What is the observed relationship between species richness and productivity // Ecology. V. 82. № 9. P. 2381–2396.
  53. Moulton C.A., Gough L., 2011. Effects of soil nutrient availability on the role of sexual reproduction in an Alaskan tundra plant community // Arctic Antarctic Alpine Res. V. 43. № 4. P. 612–620.
  54. Munoz A.A., Celedon-Neghme C., Cavieres L.A., Arroyo M.T., 2005. Bottom-up effects of nutrient availability on flower production, pollinator visitation, and seed output in a high-Andean shrub // Oecologia. V. 143. P. 126–135.
  55. Niu K., Choler P., Zhao B., Du G., 2009. The allometry of reproductive biomass in response to land use in Tibetan alpine grasslands // Funct. Ecol. V. 23. № 2. P. 274–283.
  56. Olde Venterink H., 2016. Productivity increase upon supply of multiple nutrients in fertilization experiments: co-limitation or chemical facilitation? // Plant Soil. V. 408. № 1–2. P. 515–518.
  57. Onipchenko V.G., Makarov M.I., Akhmetzhanova A.A., Soudzilovskaia N.A., Aibazova F.U., et al., 2012. Alpine plant functional group responses to fertiliser addition depend on abiotic regime and community composition // Plant Soil. V. 357. № 1–2. P. 103–115.
  58. Petraglia A., Carbognani M., Tomaselli M., 2013. Effects of nutrient amendments on modular growth, flowering effort and reproduction of snowbed plants // Plant Ecol. Divers. V. 6. № 3–4. P. 475–486.
  59. Petraglia A., Tomaselli M., Mondoni A., Brancaleoni L., Carbognani M., 2014. Effects of nitrogen and phosphorus supply on growth and flowering phenology of the snowbed forb Gnaphalium supinum L. // Flora: Morphol. Distrib. Funct. Ecol. Plants. V. 209. № 5–6. P. 271–278.
  60. Pierce S., Negreiros D., Cerabolini B.E.L., Kattge J., Díaz S., et al., 2017. A global method for calculating plant CSR ecological strategies applied across biomes world‐wide // Funct. Ecol. V. 31. № 2. P. 444–457.
  61. Ren Z., Li Q., Chu C., Zhao L., Zhang J., et al., 2010. Effects of resource additions on species richness and ANPP in an alpine meadow community // J. Plant Ecol. V. 3. № 1. P. 25–31.
  62. Samson D.A., Werk K.S., 1986. Size-dependent effects in the analysis of reproductive effort in plants // Am. Nat. V. 127. № 5. P. 667–680.
  63. Smith J., Halvorson J., Bolton H., 2002. Soil properties and microbial activity across a 500 m elevation gradient in a semi-arid environment // Soil Biol. Biochem. V. 34. P. 1749–1757.
  64. Tamm C.O., 2012. Nitrogen in Terrestrial Ecosystems: Questions of Productivity, Vegetational Changes, and Ecosystem Stability. Berlin: Springer Science & Business Media. 116 p.
  65. Tilman D., 1982. Resource Competition and Community Structure. Princeton: Princeton Univ. Press. 296 p.
  66. Tilman D., 1988. Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton: Princeton Univ. Press. 360 p.
  67. Verma P., Sagar R., 2020. Responses of diversity, productivity, and stability to the nitrogen input in a tropical grassland // Ecol. Appl. V. 30. № 2. Art. e02037.
  68. Vitousek P.M., Porder S., Houlton B.Z., Chadwick O.A., 2010. Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen–phosphorus interactions // Ecol. Appl. V. 20. № 1. P. 5–15.
  69. Ward D., 2020. Are there common assembly rules for different grasslands? Comparisons of long-term data from a subtropical grassland with temperate grasslands // J. Veg. Sci. V. 31. № 5. P. 780–791.
  70. Ward J.H., 1963. Hierarchical grouping to optimize an objective function // J. Am. Stat. Assoc. V. 58. № 301. P. 236–244.
  71. Wüst-Galley C., Volk M., Bassin S., 2021. Interaction of climate change and nitrogen deposition on subalpine pastures // J. Veg. Sci. V. 32. № 1. Art. e12946.
  72. Yang X., Chen Y., Zhang T., Zhang P., Guo Z., et al., 2023. Different responses of functional groups to N addition increased synchrony and shortened community reproductive duration in an alpine meadow // J. Ecol. V. 111. № 10. P. 2231–2244.
  73. Yang Z., Ruijven J., van, Du G., 2011. The effects of long-term fertilization on the temporal stability of alpine meadow communities // Plant Soil. V. 345. № 1–2. P. 315–324.
  74. Zheng Z., Bai W., Zhang W.-H., 2019. Root trait-mediated belowground competition and community composition of a temperate steppe under nitrogen enrichment // Plant Soil. V. 437. № 1–2. P. 341–354.

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML

Declaração de direitos autorais © Russian Academy of Sciences, 2025