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Leaf Water Relations in Epiphytic Ferns Are Driven by Drought Avoidance

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Leaf Water Relations in Epiphytic Ferns Are Driven by Drought Avoidance Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms Courtney Campany1, Jarmila Pittermann2, Alex Baer2, Helen Holmlund3, Eric Schuettpelz4, Klaus Mehltreter5, and James (Eddie) Watkins6 1Shepherd University 2University of California Santa Cruz 3Pepperdine University 4Smithsonian Institution 5Instituto de Ecologia 6Colgate University February 4, 2021 Abstract Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic, and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%), and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation, and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely canalized physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat. Hosted file epiphyte_water_relations_main.pdf available at https://authorea.com/users/393602/articles/ 507201-leaf-water-relations-in-epiphytic-ferns-are-driven-by-drought-avoidance-rather- than-tolerance-mechanisms Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 1 a Terrestrial 80 b b Hemi−epiphyte Epiphyte 1000 60 ) 2 m c ( a e r a 40 a n i m 100 a Stipe length (cm) L 20 2 Rcond = 0.24 2 Rmarg = 0.88 0 A 10 B 1 10 100 Terrestrial Hemi−epiphyte Epiphyte Stipe length (cm) 80 Terrestrial 0.20 Hemi−epiphyte a b b Epiphyte 60 0.15 4 10 x n o i t c 40 a 0.10 r f m e l y Stipe length (cm) X 20 0.05 2 Rcond = 0.33 2 Rmarg = 0.88 A 0 B 0.00 Terrestrial Hemi−epiphyte Epiphyte 0.0 0.2 0.4 0.6 0.8 −2 Total xylem areastipe (mm ) Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 2 a ab b a ab b 600 −26 500 −28 ) 2 400 − −30 m g ( C (‰) 300 13 A −32 δ M L 200 −34 100 −36 0 A B Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse−38 without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. Terrestrial Hemi−epiphyte Epiphyte Terrestrial Hemi−epiphyte Epiphyte 2 Rcond = 0.22 2 5 Rmarg = 0.79 2 1 Foliar Nitrogen (%) Foliar Terrestrial 0.5 Hemi−epiphyte Epiphyte Wright et al. 2004 C 0.2 10 100 1000 − LMA (g m 2) a b b a b ab 150 2500 ) 2 − m m ) a 2 t 2000 a m 3 u m ( o t 100 e s ( z i s y l t i 1500 a s t n a e m d o l t a S t a 50 1000 m o t S 500 0 A B Terrestrial Hemi−epiphyte Epiphyte Terrestrial Hemi−epiphyte Epiphyte 20 Terrestrial a a a Hemi−epiphyte 0.0 Epiphyte 15 −0.5 ) 1 − a P M (MPa) 10 ( P L −1.0 T Ψ Ψ 1 5 −1.5 Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 0 A B −2.0 0 5 10 15 Terrestrial Hemi−epiphyte Epiphyte 100−RWC ( %) a ab b 0.0 0.25 1.2 a ab b 1.0 ) 1 − 0.8 a P 0.20 M ( −0.5 0.6 P L T C 0.4 ) 1 − a 0.2 0.15 P M (MPa) ( o 0.0 −1.0 t f Ψ Terrestrial Hemi−epiphyte Epiphyte C 0.10 −1.5 0.05 C D −2.0 Terrestrial Hemi−epiphyte Epiphyte 0 10 20 30 40 50 60 ε (MPa) 4 Parapolystichum excultum 98 Mickelia nicotianifolia Elaphoglossum latifolium 100 100 100 Elaphoglossum herminieri 100 100 Elaphoglossum decursivum Elaphoglossum amygdalifolium 100 Polybotrya osmundacea 75 Olfersia cervina Dryopteris patula 100 Nephrolepis rivularis E1 100 100 Nephrolepis brownii Nephrolepis biserrata 100 Lomariopsis maxonii 100 100 Lomariopsis japurensis Cyclopeltis semicordata Tectaria incisa 100 Oleandra costaricensis 100 Oleandra articulata Serpocaulon triseriale 100 100 Serpocaulon loriciforme 100 72 73 Serpocaulon fraxinifolium 96 Pleopeltis bradeorum 98 Phlebodium aureum 100 Pecluma pectinata 79 Niphidium crassifolium Campyloneurum brevifolium 98 Goniopteris nicaraguensis 100 Goniopteris curta Christella dentata Diplazium prominulum 100 Diplazium striatastrum 100 100 E2 84 Diplazium atirrense Salpichlaena volubilis 100 92 Parablechnum schiedeanum 51 Blechnum occidentale 96 Asplenium uniseriale 100 Asplenium serratum 99 Asplenium juglandifolium Asplenium auritum Terrestrial 0 Stipe length (cm) 62.043 Hemi−epiphyte 0 0.02 Epiphyte nucleotide substitutions per site Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 5 Parapolystichum excultum 98 Mickelia nicotianifolia Elaphoglossum latifolium 100 100 100 Elaphoglossum herminieri 100 100 Elaphoglossum decursivum Elaphoglossum amygdalifolium 100 Polybotrya osmundacea 75 Olfersia cervina Dryopteris patula 100 Nephrolepis rivularis E1 100 100 Nephrolepis brownii Nephrolepis biserrata 100 Lomariopsis maxonii 100 100 Lomariopsis japurensis Cyclopeltis semicordata Tectaria incisa 100 Oleandra costaricensis 100 Oleandra articulata Serpocaulon triseriale 100 100 Serpocaulon loriciforme 100 72 73 Serpocaulon fraxinifolium 96 Pleopeltis bradeorum 98 Phlebodium aureum 100 Pecluma pectinata 79 Niphidium crassifolium Campyloneurum brevifolium 98 Goniopteris nicaraguensis 100 Goniopteris curta Christella dentata Diplazium prominulum 100 Diplazium striatastrum 100 100 E2 84 Diplazium atirrense Salpichlaena volubilis 100 92 Parablechnum schiedeanum 51 Blechnum occidentale 96 Asplenium uniseriale 100 Asplenium serratum 99 Asplenium juglandifolium Asplenium auritum ( −2) Terrestrial 8.7 Stomatal density stomata mm 121.6 Hemi−epiphyte 0 0.02 Epiphyte nucleotide substitutions per site Posted on Authorea 4 Feb 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.161240006.66602471/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 6.
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