Plant Ecology and Evolution 152(3): 426-436, doi: 10.5091/plecevo.2019.1525
Leaf physiological and structural plasticity of two Asplenium (Aspleniaceae) species coexisting in sun and shade conditions
expand article infoOlena Vasheka, Loretta Gratani§, Giacomo Puglielli§
‡ Department of Plant Biology, Educational and Scientific Centre “Institute of Biology and Medicine” Taras Shevchenko National University of Kyiv, 64/13, Volodymyrska Street, Kyiv, ISO 3166-2:UA-01601, Ukraine§ Department of Environmental Biology, Sapienza University of Rome, P.le A. Moro 5, Rome, ISO 3166-2:IT-00185, Italy
Open Access

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.

acclimation capability, ferns, leaf anatomy, leaf mass per area, photosynthesis, plasticity


  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Choy-Sin Y., Suan W.Y. (1974) Photosynthesis and respiration of ferns in relation to their habit. American Fern Journal 64: 40–48.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Soster M. (2001) Identikit delle Felci d’Italia. Guida al riconoscimento delle Pteridofite italiane. Valsesia Editrice.
  • 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.
  • 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., 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.