Leaf physiological and structural plasticity of two Asplenium (Aspleniaceae) species coexisting in sun and shade conditions
Cover Plant Ecology and Evolution volume 152 number3

Supplementary Files

Supplementary File 1


acclimation capability
leaf anatomy
leaf mass per area

How to Cite

Vasheka, O., Gratani, L. and Puglielli, G. (2019) “Leaf physiological and structural plasticity of two Asplenium (Aspleniaceae) species coexisting in sun and shade conditions”, Plant Ecology and Evolution, 152(3), pp. 426-436. doi: 10.5091/plecevo.2019.1525.


Background and aims – Relatively few studies have addressed the sun-shade response of fern species. Moreover, there is no information on species-specific plasticity patterns of such response, their relationship with species ecological requirements and the costs of such plasticity. The present study aims at filling these gaps by analysing the sun-shade plastic response of two Asplenium species that differ in their ecological requirements.
Methods – We measured 27 leaf morphological, anatomical and physiological parameters using standard methods for A. ceterach and A. trichomanes in the field. The parameters were combined through Principal Component Analysis in order to highlight an integrated sun-shade response across species. Linear regression analysis was carried out to highlight the relationship between the calculated species plasticity patterns and the structural control on photosynthetic process.
Key results – A significant degree of phenotypic plasticity was found for both species. Moreover, sun and shade leaves shared a common slope for the morpho-functional relationships reflecting no additional costs in terms of carbon assimilation. Even if the plastic responses of the two species scaled positively (R2 = 0.68, P = 4.667e‒07), A. trichomanes was characterized by a slightly higher anatomical plasticity (plasticity index = 0.19), while A. ceterach showed a higher physiological plasticity (0.60).
Conclusion – A remarkable acclimation capacity for the two Asplenium species in response to different light conditions was highlighted. Nevertheless, A. ceterach seems to be more suited to cope with full sunlight conditions as compared to A. trichomanes, according to species ecological requirements.



Arens N.C. (1997) Responses of leaf anatomy to light environment in the tree fern Cyathea caracasana (Cyatheaceae) and its application to some ancient seed ferns. Palaios 12: 84–94. https://doi.org/10.2307/3515296

Atkinson L.J., Campbell C.D., Zaragoza-Castells J., Hurry V., Atkin O.K. (2010) Impact of growth temperature on scaling relationships linking photosynthetic metabolism to leaf functional traits. Functional Ecology 24: 1181–1191. https://doi.org/10.1111/j.1365-2435.2010.01758.x

Bauer H., Gallmetzer Ch., Sato T. (1991) Phenology and photosynthetic activity in sterile and fertile sporophytes of Dryopteris filix-mas (L.) Schott. Oecologia 86: 159–162. https://doi.org/10.1007/BF00317526

Brach A.R., McNaughton S.J., Raynal D.J. (1993) Photosynthetic adaptability of two fern species of a Northern Hardwood forest. American Fern Journal 83: 47–53. https://doi.org/10.2307/1547566

Brodribb T.J., Holbrook N.M. (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist 162: 663–670. https://doi.org/10.1111/j.1469-8137.2004.01060.x

Chelli S., Marignani M., Barni E., Petraglia A., Puglielli G., Wellstein C., Acosta A.T.R., Bolpagni R., Bragazza L., Campetella G., Chiarucci A., Conti L., Nascimbene J., Orsenigo S., Pierce S., Ricotta C., Tardella F.M., Abeli T., Aronne G., Bacaro G., Bagella S., Benesperi R., Bernareggi G., Bonanomi G., Bricca A., Brusa G., Buffa G., Burrascano S., Caccianiga M., Calabrese V., Canullo R., Carbognani M., Carboni M., Carranza M.L., Catorci A., Ciccarelli D., Citterio S., Cutini M., Dalle Fratte M., De Micco V., Del Vecchio S., Di Martino L., Di Musciano M., Fantinato E., Filigheddu R., Frattaroli A.R., Gentili R., Gerdol R., Giarrizzo E., Giordani P., Gratani L., Incerti G., Lussu M., Mazzoleni S., Mondoni A., Montagnani C., Montagnoli A., Paura B., Petruzzellis F., Pisanu S., Rossi G., Sgarbi E., Simonetti E., Siniscalco C., Slaviero A., Stanisci A., Stinca A., Tomaselli M., Cerabolini B.E.L. (2019) Plant–environment interactions through a functional traits perspective: a review of Italian studies. Plant Biosystems. https://doi.org/10.1080/11263504.2018.1559250

Choy-Sin Y., Suan W.Y. (1974) Photosynthesis and respiration of ferns in relation to their habit. American Fern Journal 64: 40–48. https://doi.org/10.2307/1546761

de la Riva E.G., Olmo M., Poorter H., Ubera J.L., Villar R. (2016) Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. PLoS ONE 11(2): e0148788. https://doi.org/10.1371/journal.pone.0148788

Didukh Ya.P. (2011) The ecological scales for the species of Ukrainian flora and their use in synphytoindication. Kyiv, Phytosociocentre.

Durand L.Z., Goldstein G. (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126: 345–354. https://doi.org/10.1007/s004420000535

Flexas J., Scoffoni C., Gago J., Sack L. (2013) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. Journal of Experimental Botany 64: 3965–3981. https://doi.org/10.1093/jxb/ert319

Gago J., Coopman R.E., Cabrera H.M., Hermida C., Molins A., Conesa M.A., Galmés J., Ribas-Carbó M., Flexas J. (2013) Photosynthesis limitations in three fern species. Physiologia Plantarum 149: 599–611. https://doi.org/10.1111/ppl.12073

Giuliani A. (2017) The application of principal component analysis to drug discovery and biomedical data. Drug Discovery Today 22: 1069–1076. https://doi.org/10.1016/j.drudis.2017.01.005

Gratani L. (2014) Plant phenotypic plasticity in response to environmental factors. Advances in Botany 2014: 208747. https://doi.org/10.1155/2014/208747

Hallik L., Niinemets Ü., Kull O. (2012) Photosynthetic acclimation to light in woody and herbaceous species: a comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field. Plant Biology 14: 88–99. https://doi.org/10.1111/j.1438-8677.2011.00472.x

Hetherington A.M., Woodward F.I. (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901–908. https://doi.org/10.1038/nature01843

Hietz P. (2010) Fern adaptations to xeric environments. In: Mehltreter K., Walker L.R., Sharpe J.M. (eds) Fern ecology: 140–176. New York, Cambridge University Press.

John S.P., Hasenstein K.H. (2017) The role of peltate scales in desiccation tolerance of Pleopeltis polypodioides. Planta 245: 207–220. https://doi.org/10.1007/s00425-016-2631-2

Karst A.L., Lechowicz M.J. (2007) Are correlations among foliar traits in ferns consistent with those in the seed plants? New Phytologist 173: 306–312. https://doi.org/10.1111/j.1469-8137.2006.01914.x

Ludlow C.J., Wolf F.T. (1975) Photosynthesis and respiration rates of ferns. American Fern Journal 65: 43–48. https://doi.org/10.2307/1546309

Marchetti D. (2001) Pteridophite d’Italia. Annali del Museo Civico di Rovereto 19: 71–231.

Nishida K., Kodama N., Yonemura S., Hanba Y.T. (2015) Rapid response of leaf photosynthesis in two fern species Pteridium aquilinum and Thelypteris dentata to changes in CO2 measured by tunable diode laser absorption spectroscopy. Journal of Plant Research 128: 777–789. https://doi.org/10.1007/s10265-015-0736-5

Niinemets Ü., Kull O., Tenhunen J.D. (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell & Environment 27: 293–313. https://doi.org/10.1111/j.1365-3040.2003.01143.x

Nurul Hafiza M.R., Yong K.T., Osman N., Nasrulhaq-Boyce A. (2014) Leaf photosynthetic characteristics in eight shaded Malaysian filmy ferns. Phyton 83: 353–361.

Page C.N. (2002) Ecological strategies in fern evolution: a neopteridological overview. Review of Palaeobotany and Palynology 119: 1–33. https://doi.org/10.1016/S0034-6667(01)00127-0

Pignatti S (1982) Flora d’ Italia, Vol. 1. Bologna, Edagricole.

Preston C.D., Pearman D.A., Dines T.D. (2002) New Atlas of the British and Irish Flora. Oxford, Oxford University Press.

Proctor M.C.F., Tuba Z. (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytologist 156: 327–349. https://doi.org/10.1046/j.1469-8137.2002.00526.x

Pryer K.M., Schuettpelz E. (2009) Ferns (Monilophyta). In: Hedges S.B., Kumar S. (eds) The timetree of life: 153–156. Oxford, Oxford University Press.

Pteridophyte Phylogeny Group (PPG 1) (2016) A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563–603. https://doi.org/10.1111/jse.12229

Puglielli G., Varone L. (2018) Inherent variation of functional traits in winter and summer leaves of Mediterranean seasonal dimorphic species: evidence of a ‘within leaf cohort’ spectrum. AoB Plants 10(3): ply027. https://doi.org/10.1093/aobpla/ply027

Puglielli G., Varone L., Gratani L., Catoni R. (2017) Specific leaf area variations drive acclimation of Cistus salvifolius in different light environments. Photosynthetica 55: 31–40. https://doi.org/10.1007/s11099-016-0235-5

Sack L., Grubb P.J., Marañón T. (2003) The functional morphology of juvenile plants tolerant of strong summer drought in shaded forest understories in southern Spain. Plant Ecology 168: 139–163. https://doi.org/10.1023/A:1024423820136

Schlichting C.D. (1986) The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17: 667–693. https://doi.org/10.1146/annurev.es.17.110186.003315

Schneider H., Schuettpelz E., Pryer K.M., Cranfill R., Magallón S., Lupia R. (2004) Ferns diversified in the shadow of angiosperms. Nature 428: 553–557. https://doi.org/10.1038/nature02361

Soster M. (2001) Identikit delle Felci d’Italia. Guida al riconoscimento delle Pteridofite italiane. Valsesia Editrice.

Stuntz S., Zotz G. (2001) Photosynthesis in vascular epiphytes: a survey of 27 species of diverse taxonomic origin. Flora 196: 132–141. https://doi.org/10.1016/S0367-2530(17)30028-2

Tosens T., Nishida K., Gago J., Coopman R.E., Cabrera H.M., 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 Phytologyst 209: 1576–1590. https://doi.org/10.1111/nph.13719

Tutin T.G., Burges N.A., Chater A.O., Edmondson J.R., Heywood V.H., Moore D.M., Valentine D.H., Walters S.M., Webb D.A. (2010) Flora Europaea, vol. 1: Psilotaceae to Platanaceae. Cambridge, Cambridge University Press.

Valladares F., Niinemets Ü. (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39: 237–257. https://doi.org/10.1146/annurev.ecolsys.39.110707.173506

Valladares F., Wright S.J., Lasso E., Kitajima K., Pearcy R.W. (2000) Plastic phenotypic response to light of 16 congeneric shrubs from Panamanian rainforest. Ecology 8: 1925–1936.

Valladares F., Gianoli E., Gomez J.M. (2007) Ecological limits to plant phenotypic plasticity. New Phytologist 176: 749–763. https://doi.org/10.1111/j.1469-8137.2007.02275.x

Vasheka O., Puglielli G., Crescente M.F., Varone L., Gratani L. (2016) Anatomical and morphological leaf traits of three evergreen ferns (Polystichum setiferum, Polypodium interjectum and Asplenium scolopendrium). American Fern Journal 106: 258–268. https://doi.org/10.1640/0002-8444-106.4.258

Warton D.I., Duursma R.A., Falster D.S., Taskinen S. (2012) smatr3– an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x

Warton D.I., Wright I.J., Falster D.S., Westoby M. (2006) Bivariate line-fitting methods for allometry. Biological Reviews 81: 259–291. https://doi.org/10.1017/S1464793106007007

Watkins J.E., Holbrook N.M., Zwieniecki M.A. (2010) Hydraulic properties of fern sporophytes: consequences for ecological and evolutionary diversification. American Journal of Botany 97: 2007–2019. https://doi.org/10.3732/ajb.1000124

Westoby M., Reich P.B., Wright I.J. (2013) Understanding ecological variation across species: area-based vs mass-based expression of leaf traits. New Phytologist 199: 322–323. https://doi.org/10.1111/nph.12345

Winter K., Osmond C.B., Hubick K.T. (1986) Crassulacean acid metabolism in the shade. Studies on an epiphytic fern, Pyrrosia longifolia, and other rainforest species from Australia. Oecologia 68: 224–230. https://doi.org/10.1007/BF00384791

Wright I.J., Reich P.B., Westoby M. (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high and low-nutrient habitats. Functional Ecology 15: 423–434. https://doi.org/10.1046/j.0269-8463.2001.00542.x

Wright I.J., Reich P.B., Westoby M., Ackerly D.D., Baruch Z., Bongers F., Cavender-Bares J., Chapin T., Cornelissen J.H.C., Diemer M., Flexas J., Garnier E., Groom P.K., Gulias J., Hikosaka K., Lamont B.B., Lee T., Lee W., Lusk C., Midgley J.J., Navas M.L., Niinemets U., Oleksyn J., Osada N., Poorter H., Poot P., Prior L., Pyankov V.I., Roumet C., Thomas S.C., Tjoelker M.G., Veneklaas E.J., Villar R. (2004) The worldwide leaf economics spectrum. Nature 428: 821–827. https://doi.org/10.1038/nature02403

Wyka T., Robakowski P., Zytkowiak R. (2007) Acclimation of leaves to contrasting irradiance in juvenile trees differing in shade tolerance. Tree Physiology 27: 1293–1306. https://doi.org/10.1093/treephys/27.9.129

Zhang S.-B., Sun M., Cao K.-F., Hu H., Zhang J.-L. (2014) Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. PLoS One 9: e84682. https://doi.org/10.1371/journal.pone.0084682

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.