Abstract
Analysis of plant functional traits and their phylogenetic relationships has shed light on the processes structuring the occurrence patterns of angiosperm taxa across environmental gradients. In montane tropical forests, angiosperms coexist with diverse communities of terrestrial ferns, with distinct evolutionary histories, leaf morphology, and reproductive systems. Here we examined the functional traits, functional dispersion, and phylogenetic diversity of ferns across a well-described gradient of moisture and soil nutrient availability in a premontane tropical rainforest in western Panama. We measured 15 functional traits from 33 terrestrial fern species occurring in 12 one-ha plots. We applied RLQ and fourth-corner analyses to assess relationships between trait and environmental variables and used beta regression to evaluate how functional dispersion responds to environmental factors. In addition, we analyzed trait distributions with respect to fern phylogeny. We found that functional composition was predicted by soil variables and dry season rainfall. Leaf phosphorus (P) increased and leaf carbon (C) to nitrogen (N) ratio decreased with increasing soil total N:P ratio. Functional dispersion decreased with increasing soil total N:P in wet sites and with increasing manganese in dry sites, suggesting that low soil fertility and dry season moisture stress both tend to reduce functional diversity. Traits exhibited phylogenetic clustering primarily at deep nodes associated with tree versus herbaceous fern clades. Our results indicate that environmental filtering of functional traits affects ferns in a similar way to angiosperms and highlight the association of the early tree fern clade with low fertility soils.
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Viana, J.; Turner, B.; Dalling, J. (2020): Fern functional traits. The University of Illinois at Urbana–Champaign. https://doi.org/10.13012/B2IDB-8724462_V1
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References
Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141:612–619. https://doi.org/10.1007/s00442-004-1679-z
Amatangelo KL, Vitousek PM (2008) Stoichiometry of ferns in Hawaii: implications for nutrient cycling. Oecologia 157:619–627. https://doi.org/10.1007/s00442-008-1108-9
Andersen KM, Turner BL, Dalling JW (2010) Soil-based habitat partitioning in understorey palms in lower montane tropical forests. J Biogeogr 37:278–292. https://doi.org/10.1111/j.1365-2699.2009.02192.x
Andersen KM, Endara MJ, Turner BL, Dalling JW (2012) Trait-based community assembly of understory palms along a soil nutrient gradient in a lower montane tropical forest. Oecologia 168:519–531. https://doi.org/10.1007/s00442-011-2112-z
Aros-Mualin D, Noben S, Karger DN et al (2021) Functional diversity in ferns is driven by species richness rather than by environmental constraints. Front Plant Sci 11:1–11. https://doi.org/10.3389/fpls.2020.615723
Austin MP (1999) The potential contribution of vegetation ecology to biodiversity research. Ecography (cop) 22:465–484. https://doi.org/10.1111/j.1600-0587.1999.tb01276.x
Barton K (2020) MuMIn: Mulit-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn
Benson DA, Karsch-Mizrachi I, Lipman DJ et al (2009) GenBank. Nucleic Acids Res 37:D26–D31. https://doi.org/10.1093/nar/gkn723
Britton MR, Watkins JE (2016) The economy of reproduction in dimorphic ferns. Ann Bot 118:1139–1149. https://doi.org/10.1093/aob/mcw177
Burnham KP, Anderson DR (1998) Practical use of the information-theoretic approach. In: Burnham KP (ed) Model selection and inference, 2nd edn. Springer-Verlag, New York, pp 75–117
Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488. https://doi.org/10.1111/j.1472-4642.2009.00560.x
Carvajal-Hernández CI, Gómez-Díaz JA, Kessler M, Krömer T (2018) Influence of elevation and habitat disturbance on the functional diversity of ferns and lycophytes. Plant Ecol Divers 11:335–347. https://doi.org/10.1080/17550874.2018.1484526
Cavelier J, Solis D, Jaramillo MA (1996) Fog interception in montane forests across the central cordillera of Panamá. J Trop Ecol 12:357–369. https://doi.org/10.1017/s026646740000955x
Cavender-Bares J, Kitajima K, Bazzaz FA (2004) Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecol Monogr 74:635–662. https://doi.org/10.1890/03-4007
Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715. https://doi.org/10.1111/j.1461-0248.2009.01314.x
Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259. https://doi.org/10.1146/annurev.es.13.110182.001305
Chenery EM (1949) Aluminium in the plant world. Kew Bull 4:463–473. https://doi.org/10.2307/4109057
Cornelissen JHC, Lavorel S, Garnier E et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/bt02124
Cornelissen JHC, Bin SY, Yu FH, Dong M (2014) Plant traits and ecosystem effects of clonality: a new research agenda. Ann Bot 114:369–376. https://doi.org/10.1093/aob/mcu113
Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal california. Ecol Monogr 79:109–126. https://doi.org/10.1890/07-1134.1
Cribari-Neto F, Zeileis A (2010) Beta regression in R. J Stat Softw 34:1–24. https://doi.org/10.18637/jss.v034.i02
Dai X, Chen C, Li Z, Wang X (2020) Taxonomic, phylogenetic, and functional diversity of ferns at three differently disturbed sites in Longnan county. China Diversity 12:135. https://doi.org/10.3390/d12040135
Dalling JW, Prada CMM, Heineman KDD et al (2021) Introduction to the fortuna forest reserve: soil and climate effects on the tree communities of a premontane tropical forest. In: Dalling JW, Turner BL (eds) Fortuna forest reserve, panama: interacting effects of climate and soils on the biota of a wet premontane tropical forest. The Smithsonian Institution, Washington, D.C., pp 1–33
de Bello F, Berg MP, Dias ATC et al (2015) On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobot 50:349–357. https://doi.org/10.1007/s12224-015-9228-6
Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321. https://doi.org/10.1104/pp.107.2.315
Díaz S, Kattge J, Cornelissen JHC et al (2016) The global spectrum of plant form and function. Nature 529:167–171. https://doi.org/10.1038/nature16489
Dolédec S, Chessel D, ter Braak CJF, Champely S (1996) Matching species traits to environmental variables: a new three-table ordination method. Environ Ecol Stat 3:143–166. https://doi.org/10.1007/bf02427859
Dray S, Dufour AB (2007) The ade4 package: Implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04
Dray S, Legendre P (2008) Testing the species traits environment relationships: the fourth-corner problem revisited. Ecology 89:3400–3412. https://doi.org/10.1890/08-0349.1
Dray S, Chessel D, Thioulouse J (2003) Co-inertia analysis and the linking of ecological data tables. Ecology 84:3078–3089. https://doi.org/10.1890/03-0178
Dray S, Choler P, Dolédec S et al (2014) Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95:14–21. https://doi.org/10.1890/13-0196.1
El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 21:353–386. https://doi.org/10.1080/01904169809365409
Fernando DR, Lynch JP (2015) Manganese phytotoxicity: new light on an old problem. Ann Bot 116:313–319. https://doi.org/10.1093/aob/mcv111
Ferrari SLP, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815. https://doi.org/10.1080/0266476042000214501
Fine PVA, Kembel SW (2011) Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography (cop) 34:552–565. https://doi.org/10.1111/j.1600-0587.2010.06548.x
Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA): image-processing software to analyze true-color hemispherical canopy photographs, users manual and program documentation, Copyr. © 1999. Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New York
Garnier E, Cortez J, Billès G et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. https://doi.org/10.1890/03-0799
Graham MHMH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815. https://doi.org/10.1890/02-3114
Grime JP (1991) Nutrition, environment and plant ecology: an overview. In: Porter J, Lawlor D (eds) Plant growth: interactions with nutrition and environment. Cambridge University Press, Cambridge, pp 249–267
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. https://doi.org/10.1111/j.1420-9101.2010.02210.x
Hardy OJ, Senterre B (2007) Characterizing the phylogenetic structure of communities by an additive partitioning of phylogenetic diversity. J Ecol 95:493–506. https://doi.org/10.1111/j.1365-2745.2007.01222.x
Hill MO, Smith AJE (1976) Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 25:249–255. https://doi.org/10.2307/1219449
Holdridge L (1947) Determination of world plant formations from simple climatic data. Science (80) 105:367–368. https://doi.org/10.1126/science.105.2727.367
Huang JW, Grunes DL, Kochian LV (1992) Aluminum effects on the kinetics of calcium uptake into cells of the wheat root apex. Planta 188:414–421. https://doi.org/10.1007/BF00192809
Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307. https://doi.org/10.1093/biomet/76.2.297
Jager MM, Richardson SJ, Bellingham PJ et al (2015) Soil fertility induces coordinated responses of multiple independent functional traits. J Ecol 103:374–385. https://doi.org/10.1111/1365-2745.12366
Jain M, Flynn DFB, Prager CM et al (2014) The importance of rare species: a trait-based assessment of rare species contributions to functional diversity and possible ecosystem function in tall-grass prairies. Ecol Evol 4:104–112. https://doi.org/10.1002/ece3.915
Karst AL, Lechowicz MJ (2007) Are correlations among foliar traits in ferns consistent with those in the seed plants? New Phytol 173:306–312. https://doi.org/10.1111/j.1469-8137.2006.01914.x
Kembel SW, Hubbell SP (2006) The phylogenetic structure of a neotropical forest tree community. Ecology 87:86–99. https://doi.org/10.1890/0012-9658(2006)87[86:tpsoan]2.0.co;2
Kessler M, Kluge J, Hemp A, Ohlemüller R (2011) A global comparative analysis of elevational species richness patterns of ferns. Glob Ecol Biogeogr 20:868–880. https://doi.org/10.1111/j.1466-8238.2011.00653.x
Klimeš L, Klimešova J, Hendriks R, Van Groenendael J (1997) Clonal plant architecture: a comparative analysis of form and function. In: De KH, Van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 1–29
Klimešová J, Tackenberg O, Herben T (2016) Herbs are different: clonal and bud bank traits can matter more than leaf-height-seed traits. New Phytol 210:13–17. https://doi.org/10.1111/nph.13788
Kluge J, Kessler M (2011) Phylogenetic diversity, trait diversity and niches: species assembly of ferns along a tropical elevational gradient. J Biogeogr 38:394–405. https://doi.org/10.1111/j.1365-2699.2010.02433.x
Kraft NJB, Ackerly DD (2010) Functional trait and phylogenetic tests of community assembly across spatial scales in an Amazonian forest. Ecol Monogr 80:401–422. https://doi.org/10.1890/09-1672.1
Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283. https://doi.org/10.1086/519400
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Laliberté E, Norton DA, Scott D (2013) Contrasting effects of productivity and disturbance on plant functional diversity at local and metacommunity scales. J Veg Sci 24:834–842. https://doi.org/10.1111/jvs.12044
Laliberté E, Legendre P, Shipley B (2014) FD: measuring funtional diversity from multiple traits, and other tools for functional ecology. R package version 1.0–12
Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Funct Ecol 16:545–556. https://doi.org/10.1046/j.1365-2435.2002.00664.x
Legendre P, Legendre L (1998) Numerical ecology, 2nd English. Elsevier, Amsterdam
Lehtonen S, Jones MM, Zuquim G et al (2015) Phylogenetic relatedness within neotropical fern communities increases with soil fertility. Glob Ecol Biogeogr 24:695–705. https://doi.org/10.1111/geb.12294
Leibold MA, Economo EP, Peres-Neto P (2010) Metacommunity phylogenetics: separating the roles of environmental filters and historical biogeography. Ecol Lett 13:1290–1299. https://doi.org/10.1111/j.1461-0248.2010.01523.x
Leitão RP, Zuanon J, Villéger S et al (2016) Rare species contribute disproportionately to the functional structure of species assemblages. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2016.0084
Libalah MB, Droissart V, Sonké B et al (2017) Shift in functional traits along soil fertility gradient reflects non-random community assembly in a tropical African rainforest. Plant Ecol Evol 150:265–278. https://doi.org/10.5091/plecevo.2017.1318
Liu X, Swenson NG, Wright SJ et al (2012) Covariation in plant functional traits and soil fertility within two species-rich forests. PLoS ONE 7:e34767. https://doi.org/10.1371/journal.pone.0034767
Mason NWH, Richardson SJ, Peltzer DA et al (2012) Changes in coexistence mechanisms along a long-term soil chronosequence revealed by functional trait diversity. J Ecol 100:678–689. https://doi.org/10.1111/j.1365-2745.2012.01965.x
Mason NWH, De Bello F, Mouillot D et al (2013) A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J Veg Sci 24:794–806. https://doi.org/10.1111/jvs.12013
Mayfield MM, Levine JM (2010) Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecol Lett 13:1085–1093. https://doi.org/10.1111/j.1461-0248.2010.01509.x
Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348. https://doi.org/10.1046/j.1469-8137.2002.00477.x
Ordoñez JC, Van Bodegom PM, Witte JPM et al (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
Pausas JG, Verdú M (2010) The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. Bioscience 60:614–625. https://doi.org/10.1525/bio.2010.60.8.7
Pavoine S, Baguette M, Bonsall MB (2010) Decomposition of trait diversity among the nodes of a phylogenetic tree. Ecol Monogr 80:485–507. https://doi.org/10.1890/09-1290.1
Pavoine S, Gasc A, Bonsall MB, Mason NWH (2013) Correlations between phylogenetic and functional diversity: Mathematical artefacts or true ecological and evolutionary processes? J Veg Sci 24:781–793. https://doi.org/10.1111/jvs.12051
Peng S, Krieg DR, Girma FS (1991) Leaf photosynthetic rate is correlated with biomass and grain production in grain sorghum lines. Photosynth Res 28:1–7. https://doi.org/10.1007/BF00027171
Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758. https://doi.org/10.1111/j.1461-0248.2006.00924.x
Podani J (1999) Extending Gower’s general coefficient of similarity to ordinal characters. Taxon 48:331–340. https://doi.org/10.2307/1224438
Prada CM, Morris A, Andersen KM et al (2017) Soils and rainfall drive landscape-scale changes in the diversity and functional composition of tree communities in premontane tropical forest. J Veg Sci 28:859–870. https://doi.org/10.1111/jvs.12540
Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43. https://doi.org/10.1016/0040-5809(82)90004-1
Richardson SJ, Walker LR (2010) Nutrient ecology of ferns. Fern ecology. Cambridge University Press, New York, pp 111–139
Scheiner SM, Kosman E, Presley SJ, Willig MR (2017) Decomposing functional diversity. Methods Ecol Evol 8:809–820. https://doi.org/10.1111/2041-210x.12696
Schellenberger Costa D, Gerschlauer F, Pabst H et al (2017) Community-weighted means and functional dispersion of plant functional traits along environmental gradients on Mount Kilimanjaro. J Veg Sci 28:684–695. https://doi.org/10.1111/jvs.12542
Schmitt M, Watanabe T, Jansen S (2016) The effects of aluminium on plant growth in a temperate and deciduous aluminium accumulating species. AoB Plants. https://doi.org/10.1093/aobpla/plw065
Schmitt M, Mehltreter K, Sundue M et al (2017) The evolution of aluminum accumulation in ferns and lycophytes. Am J Bot 104:573–583. https://doi.org/10.3732/ajb.1600381
Spasojevic MJ, Suding KN (2012) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661. https://doi.org/10.1111/j.1365-2745.2011.01945.x
Tanaka T, Sato T (2015) Taxonomic, phylogenetic and functional diversities of ferns and lycophytes along an elevational gradient depend on taxonomic scales. Plant Ecol 216:1597–1609. https://doi.org/10.1007/s11258-015-0543-z
Team R Development Core (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJ
Tuomisto H, Poulsen AD (1996) Influence of edaphic specialization on pteridophyte distribution in neotropical rain forests. J Biogeogr 23:283–293. https://doi.org/10.1046/j.1365-2699.1996.00044.x
Tuomisto H, Ruokolainen K, Poulsen AD et al (2002) Distribution and diversity of pteridophytes and melastomataceae along edaphic gradients in Yasuní National Park, Ecuadorian Amazonia. Biotropica 34:516–533. https://doi.org/10.1111/j.1744-7429.2002.tb00571.x
Turner BL, Dalling JW (2021) Soils of the fortuna forest reserve. In: Dalling JW, Turner BL (eds) Fortuna forest reserve, panama: interacting effects of climate and soils on the biota of a wet premontane tropical forest. The Smithsonian Institution, Washington, D.C., pp 47–135
Valladares F, Gianoli E, Gómez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763. https://doi.org/10.1111/j.1469-8137.2007.02275.x
Viana JL, Dalling JW (2021) Diversity and ecology of the ferns in Fortuna. In: Dalling JW, Turner BL (eds) Fortuna forest reserve, panama: interacting effects of climate and soils on the biota of a wet premontane tropical forest. The Smithsonian Institution, Washington, D.C., pp 237–270
Viana JL, Turner BL, Dalling JW (2020) Compositional variation in understorey fern and palm communities along a soil fertility and rainfall gradient in a lower montane tropical forest. J Veg Sci 32:1–14. https://doi.org/10.1111/jvs.12947
Vitousek PM, Aplet G, Turner D, Lockwood JJ (1992) The Mauna Loa environmental matrix: foliar and soil nutrients. Oecologia 89:372–382. https://doi.org/10.1007/BF00317415
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Weiher E, Keddy PA (1995) Assembly rules, null models, and trait dispersion: new questions from old patterns. Oikos 74:159–164. https://doi.org/10.2307/3545686
Weiher E, Werf A, Thompson K et al (1999) Challenging theophrastus: a common core list of plant traits for functional ecology. J Veg Sci 10:609–620. https://doi.org/10.2307/3237076
Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227. https://doi.org/10.1023/a:1004327224729
Westoby M, Falster DS, Moles AT et al (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159. https://doi.org/10.1146/annurev.ecolsys.33.010802.150452
Wright IJ, Reich PB, 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. Funct Ecol 15:423–434. https://doi.org/10.1046/j.0269-8463.2001.00542.x
Wright IJ, Reich P, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Zemunik G, Davies SJ, Turner BL (2018) Soil drivers of local-scale tree growth in a lowland tropical forest. Ecology 99:2844–2852. https://doi.org/10.1002/ecy.2532
Zemunik G, Winter K, Turner BL (2020) Toxic effects of soil manganese on tropical trees. Plant Soil 453:343–354. https://doi.org/10.1007/s11104-020-04603-3
Zhu SD, Li RH, Song J et al (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
Acknowledgements
The authors thank Dr. Astrid Ferrer for advice with the phylogenetic tree, Carlos Espinosa and Evidelio García for field assistance, and Ben Turner and the Smithsonian Tropical Research Institute Soils Lab for assistance in the analysis of soils samples.
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The Brazilian National Council for Scientific and Technological Development (CNPq), Smithsonian Tropical Research Institute in Panama, and the Center for Latin American and Caribbean Studies at the University of Illinois at Urbana–Champaign provided funding for this research.
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JLV and JWD conceived and designed the experiment. JLV conducted fieldwork and analyzed the data. JLV and JWD wrote the manuscript.
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Viana, J.L., Dalling, J.W. Soil fertility and water availability effects on trait dispersion and phylogenetic relatedness of tropical terrestrial ferns. Oecologia 198, 733–748 (2022). https://doi.org/10.1007/s00442-022-05131-w
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DOI: https://doi.org/10.1007/s00442-022-05131-w