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Contrasting effects of light, soil chemistry and phylogeny on leaf nutrient concentrations in cave-dwelling plants

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Abstract

Background and aims

The drivers of variations in leaf nutrient concentrations in cave-dwelling plants remain poorly understood. We aimed to explore the effects of light, soil chemistry and phylogeny on leaf nutrient concentrations in cave-dwelling plants.

Methods

We quantified light availability and sampled top-soils and leaves of the co-existing herbs and ferns in three caves. We used the traditional and phylogenetic comparative methods to determine the effects of light, soil chemistry and phylogeny on leaf nutrient concentrations and the cross-species correlations between leaf nutrients.

Results

Leaf nutrient concentrations differed little among caves due to the non-significant relationships of leaf nutrient concentrations with light availability and soil nutrient concentrations across caves. The phylogenetic signals in leaf nutrient concentrations were significant for Ca, Mg and N but non-significant for the remaining nutrients. The evolutionary rates of leaf nutrient concentrations tended to increase with decreasing phylogenetic signals and were faster in herbs than ferns. These contrasting degrees of phylogenetic conservatism in leaf nutrient concentrations were best generated by Ornstein-Uhlenbeck models, i.e., stabilizing selection towards an optimum across species for P, K, S, Fe, Mn and Zn or higher optimal concentrations in herbs than ferns for Ca, Mg and N. Strong cross-species correlations between leaf nutrient concentrations such as Ca vs Mg and N vs P were found.

Conclusions

Leaf nutrient concentrations in cave-dwelling plants showed convergent adaptations to cave environments and presented contrasting degrees of phylogenetic conservatism to produce leaf nutritional diversity for the co-existing herbs and ferns in caves.

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References

  1. Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Evol Syst 39:153–170. https://doi.org/10.1146/annurev.ecolsys.39.110707.173515

  2. Bai K, Lv S, Ning S, Zeng D, Guo Y, Wang B (2019) Leaf nutrient concentrations associated with phylogeny, leaf habit and soil chemistry in tropical karst seasonal rainforest tree species. Plant Soil 434:305–326. https://doi.org/10.1007/s1104-018-3858-4

  3. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are labile. Evolution 57:717–745. https://doi.org/10.1554/0014-3820(2003)057

  4. Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33. https://doi.org/10.1017/S0021859600021572

  5. Burson A, Stomp M, Greenwell E, Grosse J, Huisman J (2018) Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community. Ecology 99:1108–1118. https://doi.org/10.1002/ecy.2187

  6. Chen H, Li D, Xiao K, Wang K (2018) Soil microbial processes and resource limitation in karst and non-karst forests. Funct Ecol 32:1400–1409. https://doi.org/10.1111/1365-2435.13069

  7. Clavel J (2018) Multivariate comparative tools for fitting evolutionary models to morphometric data. https://github.com/JClavel/mvMORPH. Accessed 31 July 2018

  8. Clavel J, Escarguel G, Merceron G (2015) mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Methods Ecol Evol 6:1311–1319. https://doi.org/10.1111/2041-210X.12420

  9. Cooper N, Jetz W, Freckleton RP (2010) Phylogenetic comparative approaches for studying niche conservatism. J Evol Biol 23:2529–2539. https://doi.org/10.1111/j.1420-9101.2010.02144x

  10. de la Riva EG, Villar R, Pérez-Ramos IG, Quero JL, Matías L, Poorter L, Marañón T (2018) Relationships between leaf mass per area and nutrient concentrations in 98 Mediterranean woody species are determined by phylogeny, habitat and leaf habit. Trees 32:497–510. https://doi.org/10.1007/s00468-017-1646-z

  11. Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95. https://doi.org/10.1016/j.tree.2010.11.011

  12. Felsenstein J (1973) Maximum-likelihood estimation of evolutionary trees from continuous characters. Am J Hum Genet 25:471–492

  13. Fernández-Martínez M, Llusià J, Filella I, Niinemets Ü, Arneth A, Wright IJ, Lereto F, Peñuelas J (2018) Nutrient-rich plants emit a less intense blend of volatile isoprenoids. New Phytol 220:773–784. https://doi.org/10.1111/nph.14889

  14. Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R (2010) Evidence of the 'plant economics spectrum' in a subarctic flora. J Ecol 98:362–373. https://doi.org/10.1111/j.1365-2745.2009.01615.x

  15. Funk JL, Amatangelo KL (2013) Physiological mechanisms drive differing foliar calcium content in ferns and angiosperms. Oecologia 173:23–32. https://doi.org/10.1007/s00442-013-2591-1

  16. Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235. https://doi.org/10.1093/molbev/mst012

  17. Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796. https://doi.org/10.1111/j.1461-0248.2011.01641.x

  18. Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341–1351. https://doi.org/10.1111/j.1558-5646.1997.tb01457.x

  19. Hao Z, Kuang Y, Kang M (2015) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29:165–176. https://doi.org/10.1111/1365-2435.12344

  20. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131. https://doi.org/10.1093/bioinformatics/btm538

  21. Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller S, White P (2012) Functions of macronutrients. In: Marschner P (ed) Marschner's mineral nutrition of higher plants,3rd edn. Academic Press, London, pp135–178

  22. Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behavior, ecology and life history. Philos T R Soc B: Biol Sci 368:20120341. https://doi.org/10.1098/rstb.2012.0341

  23. Keenan TF, Niinemets Ü (2016) Global leaf trait estimates biased due to plasticity in the shade. Nature Plants 3:16201. https://doi.org/10.1038/nplants2016.201

  24. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166

  25. Liang KM, Lin ZF, Ren H, Liu N, Zhang QM, Wang J, Wang ZF, Guan LL (2010) Characteristics of sun- and shade-adapted populations of an endangered plant Primulina tabacum hance. Photosynthetica 48:494–506

  26. Mammola S (2019) Finding answers in the dark: caves as models in ecology fifty years after Poulson and White. Ecography 42:1331–1351. https://doi.org/10.1111/ecog.03905

  27. Markesteijn L, Poorter L, Bongers F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am J Bot 94:515–525. https://doi.org/10.3732/ajb.94.4.515

  28. Monro AK, Bystriakova N, Fu L, Wen F, Wei Y (2018) Discovery of a diverse cave flora in China. PLoS One 13(2):e0190801. https://doi.org/10.1371/journal.pone.0190801

  29. Neugebauer K, Broadley MR, El-Serehy HA, George TS, McNicol JW, Moraes MF, White PJ (2018) Variation in the angiosperm ionome. Physiol Plant 163:306–322. https://doi.org/10.1111/ppl.12700

  30. Northup DE, Lavoie KH (2001) Geomicrobiology of caves: a review. Geomicrobiol J 18:199–222. https://doi.org/10.1080/01490450152467750

  31. Ordoñez JC, van Bodegom PM, Witte JM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149. https://doi.org/10.1111/j.1466-8238.2008.00441.x

  32. Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Issac JB, Pearse W (2012) Caper: comparative analyses of phylogenetics and evolution in R. Methods Ecol Evol 3:145–151

  33. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. https://doi.org/10.1038/44766

  34. Parise M, De Waele J, Gutierrez F (2009) Current perspectives on the environmental impacts and hazards in karst. Environ Geol 58:235–237. https://doi.org/10.1007/s00254-008-1608-2

  35. Poorter H, Niinemets Ü, Ntagkas N, Siebenkäs A, Mäenpää M, Matsubara S, Pons TL (2019) A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytol 223:1073–1105. https://doi.org/10.1111/nph.15754

  36. Prinzing A, Durka W, Klotz S, Brandl R (2001) The niche of higher plants: evidence for phylogenetic conservatism. Proc R Soc Lond B 268:2383–2389. https://doi.org/10.1098/rspb.2001.1801

  37. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org. Accessed 2018-07-02

  38. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperture and latitude. P Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101

  39. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591–601. https://doi.org/10.1080/10635150802302427

  40. Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light: relationships with light demand and adult stature. Funct Ecol 20:207–216. https://doi.org/10.1111/j.1365-2435.2006.01105.x

  41. Sardans J, Janssens IA, Alonso R, Veresoglou SD, Rillig G, Peñuelas J (2015) Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Glob Ecol Biogeogr 24:240–255. https://doi.org/10.1111/geb.12253

  42. Stein RJ, Höreth S, de Melo JRF, Syllwasschy L, Lee G, Garbin M (2017) Relationships between soil and leaf mineral composition are element-specific, environmental-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286. https://doi.org/10.1111/nph.14219

  43. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies using the neighbor-joining method. Proc Natl Acad Sci 101:11030–11035. https://doi.org/10.1073/pnas.0404206101

  44. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

  45. Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, Talts E, Tomas M, Hanba Y, Niinemets Ü, Flexas J (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590. https://doi.org/10.1111/nph.13719

  46. Tung Ho LS, Ané C (2014) A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst Biol 63:397–408. https://doi.org/10.1093/sysbio/syu005

  47. Verboom GA, Stock WD, Cramer MD (2017) Specialization to extremely low-nutrient soils limits the nutrittional adapability of plant lineages. Am Nat 189:684–699. https://doi.org/10.1086/691449

  48. Waite M, Sack L (2011) Does global stoichiometric theory apply to bryophytes? Tests across an elevation × soil age ecosystem matrix on Mauna Loa, Hawaii. J Ecol 99:122–134. https://doi.org/10.1111/j.1365-2745.2010.01746.x

  49. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291. https://doi.org/10.1017/S1464793106007007

  50. White PJ, Broadley MR, Thompson JA, McNicol JW, Crawley MJ, Poulton PR, Jonston AE (2012) Testing the distinctness of shoot ionomes of angiosperm families using the Rothamsted Park grass continuous Hay experiment. New Phytol 196:101–109. https://doi.org/10.1111/j.1469-8137.2012.04228.x

  51. White PJ, Broadley MR, El-Serehy HA, George TS, Neugebauer K (2018) Linear relationships between shoot magnesium and calcium concentrations among angiosperm species are associated with cell wall chemistry. Ann Bot. https://doi.org/10.1093/aob/mcy062

  52. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 18:131–146. https://doi.org/10.1080/00103628709367806

  53. Zhang SB, Zhang JL, Slik JWF, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818. https://doi.org/10.1111/j.1466-8238.2011.00729.x

  54. Zhu SD, Li RH, Song J, He PC, Liu H, Berninger F, Ye Q (2016) Different leaf cost-benefit strategies of ferns distributed in contrasting light habitats of sub-tropical forests. Ann Bot 117:497–506. https://doi.org/10.1093/aob/mcv179

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Acknowledgements

This research was supported by the Guangxi Natural Science Foundation (2013GXNSFBA019079), Guangxi Scientific and Technological Project (1355007-3) and National Natural Science Foundation (31570307; 31860042; 31860174) in China. Special thanks to the anonymous reviewers and the responsible editor (Alfonso Escudero) for providing insightful comments on the early versions of the manuscript.

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Correspondence to Kundong Bai.

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Bai, K., Wei, Y., Zhang, D. et al. Contrasting effects of light, soil chemistry and phylogeny on leaf nutrient concentrations in cave-dwelling plants. Plant Soil (2020) doi:10.1007/s11104-020-04422-6

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Keywords

  • Cave-dwelling plants
  • Leaf nutrient concentrations
  • Phylogenetic conservatism
  • Light
  • Soil chemistry
  • Phylogenetic comparative methods
  • Stabilizing selection