Tropical terrestrial and epiphytic ferns have different leaf stoichiometry with ecological implications

References

• Ågren GI, Weih M. 2012. Plant stoichiometry at different scales: element concentration patterns reflect environment more than genotype. New Phytol. 194(4):944–952. doi: 10.1111/j.1469-8137.2012.04114.x.
   PubMed Web of Science ®Google Scholar
• Allen SE, Grimshaw HM, Parkinson JA, Quarmby C. 1989. Chemical analysis of ecological materials. Oxford, UK: blackwell Scientific Publications
   Google Scholar
• Amatangelo KL, Vitousek PM. 2009. Contrasting predictors of fern versus angiosperm decomposition in a common garden. Biotropica. 41(2):154–161. doi: 10.1111/j.1744-7429.2008.00470.x.
   Web of Science ®Google Scholar
• Amatangelo KL, Vitousek PM. 2008. Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia. 157(4):619–627. doi: 10.1007/s00442-008-1108-9.
   PubMed Web of Science ®Google Scholar
• Baribault TW, Kobe RK, Finley AO. 2012. Tropical tree growth is correlated with soil phosphorus, potassium, and calcium, though not for legumes. Ecol Monogr. 82(2):189–203. doi: 10.1890/11-1013.1.
   Google Scholar
• Benner JW, Conroy S, Lunch CK, Toyoda N, Vitousek PM. 2007. Phosphorus fertilization increases the abundance and nitrogenase activity of the cyanolichen Pseudocyphellaria crocata in Hawaiian montane forests. Biotropica. 39(3):400–405. doi: 10.1111/j.1744-7429.2007.00267.x.
   Web of Science ®Google Scholar
• Benner JW, Vitousek PM. 2007. Development of a diverse epiphyte community in response to phosphorus fertilization. Ecol Lett. 10(7):628–636. doi: 10.1111/j.1461-0248.2007.01054.x.
   PubMed Web of Science ®Google Scholar
• Blanca MJ, Alarcón R, Arnau J, Bono R, Bendayan R. 2017. Non-normal data : is ANOVA still a valid option? Psicothema. 29:552–557. doi: 10.7334/psicothema2016.383.
   PubMed Web of Science ®Google Scholar
• Brodribb TJ, Holbrook NM. 2004. Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol. 162(3):663–670. doi: 10.1111/j.1469-8137.2004.01060.x.
   PubMed Web of Science ®Google Scholar
• Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS. 2009. Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol. 183(3):839–847. doi: 10.1111/j.1469-8137.2009.02844.x.
   PubMed Web of Science ®Google Scholar
• Cardelús CL, Mack MC. 2010. The nutrient status of epiphytes and their host trees along an elevational gradient in Costa Rica. Plant Ecol. 207(1):25–37. doi: 10.1007/s11258-009-9651-y.
   Web of Science ®Google Scholar
• Castellanos AE, Llano-Sotelo JM, Machado-Encinas LI, López-Piña JE, Romo-Leon JR, Sardans J, Peñuelas J. 2018. Foliar C, N, and P stoichiometry characterize successful plant ecological strategies in the Sonoran Desert. Plant Ecol. 219(7):775–788. doi: 10.1007/s11258-018-0833-3.
   Web of Science ®Google Scholar
• Chen LC, Wang LJ, Martin CE, Lin TC. 2019. Mediation of stemflow water and nutrient availabilities by epiphytes growing above other epiphytes in a subtropical forest. Ecohydrology. 12(7):1–10. doi: 10.1002/eco.2140.
   Web of Science ®Google Scholar
• Cicuzza D. 2021. Rare Pteridophytes are disproportionately frequent in the tropical forest of Xishuangbanna, Yunnan, China. Acta Oecologica. 110:103717. doi: 10.1016/j.actao.2021.103717.
   Web of Science ®Google Scholar
• Coomes DA, Allen RB, Bentley WA, Burrows LE, Canham CD, Fagan L, Forsyth DM, Gaxiola-Alcantar A, Parfitt RL, Ruscoe WA, et al. 2005. The hare, the tortoise and the crocodile: the ecology of angiosperm dominance, conifer persistence and fern filtering. J Ecology. 93(5):918–935. doi: 10.1111/j.1365-2745.2005.01012.x.
   Web of Science ®Google Scholar
• Davies SJ, Peter B. 1996. Floristic composition and stand structure of mixed dipsterocarp and heath forest in Brunei Darussalam. J Trop For Sci. 8:542–569.
   Google Scholar
• Din H, Metali F, Sukri RS. 2015. Tree diversity and community composition of the tutong white sands, Brunei darussalam: a rare tropical heath forest ecosystem. Int J Ecol. 2015:1–10. doi: 10.1155/2015/807876.
   Google Scholar
• Güsewell S. 2004. N: p ratios in terrestrial plants: variation and functional significance. New Phytol. 164(2):243–266. doi: 10.1111/j.1469-8137.2004.01192.x.
   PubMed Web of Science ®Google Scholar
• Han W, Tang L, Chen Y, Fang J. 2013. Relationship between the relative limitation and resorption efficiency of nitrogen vs. phosphorus in woody plants. PLOS One. 8(12):e83366. doi: 10.1371/journal.pone.0083366.
   PubMed Web of Science ®Google Scholar
• Hargis H, Gotsch SG, Porada P, Moore GW, Ferguson B, Van Stan JT. 2019. Arboreal epiphytes in the soil-atmosphere interface: how often are the biggest “buckets” in the canopy empty? Geosciences. 9(8):342. doi: 10.3390/geosciences9080342.
   Web of Science ®Google Scholar
• Hermans C, Vuylsteke M, Coppens F, Cristescu SM, Harren FJM, Inzé D, Verbruggen N. 2010. Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol. 187(1):132–144. doi: 10.1111/j.1469-8137.2010.03257.x.
   PubMed Web of Science ®Google Scholar
• Huang GZ, Lin TC. 2016. Response of two epiphyte species to nitrogen and phosphorus fertilization at a humid subtropical rainforest in northeastern Taiwan. Taiwan J Forest Sci. 31:293–304.
   Google Scholar
• Huang JB, Liu WY, Li S, Song L, Lu HZ, Shi XM, Chen X, Hu T, Liu S, Liu T. 2019. Ecological stoichiometry of the epiphyte community in a subtropical forest canopy. Ecol Evol. 9(24):14394–14406. doi: 10.1002/ece3.5875.
   PubMed Web of Science ®Google Scholar
• Islam SN, Mohamad SMBH, Azad AK. 2019. Acacia spp.: invasive trees along the Brunei Coast, Borneo. Coastal Research Library; Impacts of Invasive Species on Coastal Environments Coastal Research Library, vol. 29. Cham: Springer; p. 455–476. doi: 10.10007/978-3-319-91382-7_14.
   Google Scholar
• Koerselman W, Meuleman AFM. 1996. The vegetation N: p ratio: a New tool to detect the nature of nutrient limitation. J Appl Ecol. 33(6):1441. doi: 10.2307/2404783.
   Web of Science ®Google Scholar
• Lin CY, Yeh DM. 2008. Potassium nutrition affects leaf growth, anatomy, and macroelements of Guzmania. horts. 43(1):146–148. doi: 10.21273/HORTSCI.43.1.146.
   Web of Science ®Google Scholar
• Metali F, Salim KA, Tennakoon K, Burslem DFRP. 2015. Controls on foliar nutrient and aluminium concentrations in a tropical tree flora : phylogeny, soil chemistry and interactions among elements. New Phytol. 205(1):280–292. doi: 10.1111/nph.12987.
   PubMed Web of Science ®Google Scholar
• Oddo E, Inzerillo S, La Bella F, Grisafi F, Salleo S, Nardini A. 2011. Short-term effects of potassium fertilization on the hydraulic conductance of Laurus nobilis L. Tree Physiol. 31(2):131–138. doi: 10.1093/treephys/tpq115.
   PubMed Web of Science ®Google Scholar
• Praveen A, Pandey VC. 2020. Pteridophytes in phytoremediation. Environ Geochem Health. 42(8):2399–2411. doi: 10.1007/s10653-019-00425-0.
   PubMed Web of Science ®Google Scholar
• Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C. 2016. Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front Plant Sci. 7:327. doi: 10.3389/fpls.2016.00327.
   PubMed Web of Science ®Google Scholar
• Raux PS, Gravelle S, Dumais J. 2020. Design of a unidirectional water valve in Tillandsia. Nat Commun. 11(1):1–7. doi: 10.1038/s41467-019-14236-5.
   PubMed Web of Science ®Google Scholar
• Razaq M, Zhang P, Shen H-L, Salahuddin. 2017. Influence of nitrogen and phosphorous on the growth and root morphology of Acer mono. PLOS One, 212:e0171321. doi: 10.1371/journal.pone.0171321.
   PubMed Web of Science ®Google Scholar
• Richardson SJ, Walker LR. 2010. Nutrient ecology of ferns. In: Fern ecology; p. 111–139.
   Google Scholar
• Sardans J, Alonso R, Carnicer J, Fernández-Martínez M, Vivanco MG, Peñuelas J. 2016. Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain. Perspect Plant Ecol Evol Syst. 18:52–69. doi: 10.1016/j.ppees.2016.01.001.
   Web of Science ®Google Scholar
• Sardans J, Peñuelas J. 2014. Climate and taxonomy underlie different elemental concentrations and stoichiometries of forest species: the optimum. Plant Ecol. 215(4):441–455. doi: 10.1007/s11258-014-0314-2.
   PubMed Web of Science ®Google Scholar
• Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R. 2004. Ferns diversified in the shadow of angiosperms. Nature. 428(6982):553–557. doi: 10.1038/nature02361.
   PubMed Web of Science ®Google Scholar
• Schuettpelz E, Schneider H, Smith AR, Hovenkamp P, Prado J, Rouhan G, Salino A, Sundue M, Almeida TE, Parris B, et al. 2016. A community-derived classification for extant lycophytes and ferns. J Syst Evol. 54:563–603. doi: 10.1111/jse.12229.
   Web of Science ®Google Scholar
• Song WY, Zhang Z, Bin Shao HB, Guo XL, Cao HX, Zhao H, Bin Fu ZY, Hu XJ. 2008. Relationship between calcium decoding elements and plant abiotic-stress resistance. Int J Biol Sci. 4(2):116–125. doi: 10.7150/ijbs.4.116.
   PubMed Web of Science ®Google Scholar
• Stefano M, Papini A, Brighigna L. 2008. A new quantitative classification of ecological types in the bromeliad genus Tillandsia (Bromeliaceae) based on trichomes. Rev Biol Trop. 45(1):191–203.
   Google Scholar
• Suhaimi N, Cicuzza D. 2020. the effects of drought and the recovery phase of two tropical epiphytic ferns. Plant Physiol. 12:33–41.
   Google Scholar
• Sun L, Zhang B, Wang B, Zhang G, Zhang W, Zhang B, Chang S, Chen T, Liu G. 2017. Leaf elemental stoichiometry of Tamarix Lour. species in relation to geographic, climatic, soil, and genetic components in China. Ecol Eng. 106:448–457. doi: 10.1016/j.ecoleng.2017.06.018.
   Web of Science ®Google Scholar
• Suriyagoda LDB, Rajapaksha R, Pushpakumara G, Lambers H. 2018. Nutrient resorption from senescing leaves of epiphytes, hemiparasites and their hosts in tropical forests of Sri Lanka. J Plant Ecol. 11(6):815–826. doi: 10.1093/jpe/rtx049.
   Web of Science ®Google Scholar
• Testo W, Sundue M. 2016. A 4000-species dataset provides new insight into the evolution of ferns. Mol Phylogenet Evol. 105:200–211. doi: 10.1016/j.ympev.2016.09.003.
   PubMed Web of Science ®Google Scholar
• Tong R, Zhou B, Jiang L, Ge X, Cao Y, Yang Z. 2019. Leaf nitrogen and phosphorus stoichiometry of chinese fir plantations across China: a meta-analysis. Forests. 10(11):945. doi: 10.3390/f10110945.
   Web of Science ®Google Scholar
• Umana NH-N, Wanek W. 2010. Large canopy exchange fluxes of inorganic and organic nitrogen and preferential retention of nitrogen by epiphytes in a tropical lowland rainforest. Ecosystems. 13(3):367–381. doi: 10.1007/s10021-010-9324-7.
   Web of Science ®Google Scholar
• Watkins JE, Cardelús CL. 2012. Ferns in an angiosperm world: cretaceous radiation into the epiphytic niche and diversification on the forest floor. Int J Plant Sci. 173(6):695–710. doi: 10.1086/665974.
   Web of Science ®Google Scholar
• Watkins JE, Philip J, Cardelús CL. 2007. The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. Oecologia. 153(2):225–232. doi: 10.1007/s00442-007-0723-1.
   PubMed Web of Science ®Google Scholar
• White PJ, Broadley MR. 2003. Calcium in plants. Ann Bot. 92(4):487–511. doi: 10.1093/aob/mcg164.
   PubMed Web of Science ®Google Scholar
• White PJ, Brown PH. 2010. Plant nutrition for sustainable development and global health. Ann Bot. 105(7):1073–1080. doi: 10.1093/aob/mcq085.
   PubMed Web of Science ®Google Scholar
• Winkler U, Zotz G. 2010. “And then there were three”: highly efficient uptake of potassium by foliar trichomes of epiphytic bromeliads. Ann Bot. 106(3):421–427. doi: 10.1093/aob/mcq120.
   PubMed Web of Science ®Google Scholar
• Winkler U, Zotz G. 2009. Highly efficient uptake of phosphorus in epiphytic bromeliads. Ann Bot. 103(3):477–484. doi: 10.1093/aob/mcn231.
   PubMed Web of Science ®Google Scholar
• Zheng S, Shangguan Z. 2007. Spatial patterns of leaf nutrient traits of the plants in the Loess Plateau of China. Trees Struct Funct. 21(3):357–370. doi: 10.1007/s00468-007-0129-z.
   Web of Science ®Google Scholar
• Zotz G. 2016. Plants on plants – the biology of vascular epiphytes. Springer.
   Google Scholar
• Zotz G. 2004. The resorption of phosphorus is greater than that of nitrogen in senescing leaves of vascular epiphytes from lowland Panama. J Trop Ecol. 20(6):693–696. doi: 10.1017/S0266467404001889.
   Google Scholar
• Zotz G, Hietz P. 2001. The physiological ecology of vascular epiphytes: current knowledge, open questions. J Exp Bot. 52(364):2067–2078. doi: 10.1093/jexbot/52.364.2067.
   PubMed Web of Science ®Google Scholar
• Zotz G, Richter A. 2006. Changes in carbohydrate and nutrient contents throughout a reproductive cycle indicate that phosphorus is a limiting nutrient in the epiphytic bromeliad, Werauhia sanguinolenta. Ann Bot. 97(5):745–754. doi: 10.1093/aob/mcl026.
   PubMed Web of Science ®Google Scholar
• Zuquim G, Tuomisto H, Jones MM, Prado J, Figueiredo FOG, Moulatlet GM, Costa FRC, Quesada CA, Emilio T. 2014. Predicting environmental gradients with fern species composition in Brazilian Amazonia. J Veg Sci. 25(5):1195–1207. doi: 10.1111/jvs.12174.
   Web of Science ®Google Scholar