Local drivers of heterogeneity in a tropical forest: epiphytic tank bromeliads affect the availability of soil resources and conditions and indirectly affect the structure of seedling communities
Tóm tắt
Environmental heterogeneity is a key component in explaining the megadiversity of tropical forests. Despite its importance, knowledge about local drivers of environmental heterogeneity remains a challenge for ecologists. In Neotropical forests, epiphytic tank bromeliads store large amounts of water and nutrients in the tree canopy, and their tank overflow may create nutrient-rich patches in the soil. However, the effects of this nutrient flux on environmental heterogeneity and plant community structure in the understory remain unexplored. In a Brazilian coastal sandy forest, we investigated the effects of the presence of epiphytic tank bromeliads on throughfall chemistry, soil chemistry, soil litter biomass, light, and seedling community structure. In the presence of epiphytic tank bromeliads, the throughfall nitrogen concentration increased twofold, the throughfall phosphorus concentration increased threefold, and the soil patches had a 3.96% higher pH, a 50% higher calcium concentration, and 11.88% less light. By altering the availability of soil resources and conditions, the presence of bromeliads partially shifted the available niche spaces for plant species and indirectly affected the structure of the seedling communities, decreasing their diversity, density, and biomass. For the first time, we showed that the presence of tank bromeliads in the canopy can create characteristic soil patches in the understory, affecting the structure of seedling communities via fertilization. Our results reveal a novel local driver of environmental heterogeneity, reinforcing and expanding the key role of tank bromeliads both in nutrient cycling and plant community structuring of Neotropical coastal sandy forests.
Tài liệu tham khảo
Amundrud SL, Srivastava DS (2016) Trophic interactions determine the effects of drought on an aquatic ecosystem. Ecology 97:1475–1483. https://doi.org/10.1890/15-1638.1
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641. https://doi.org/10.1016/j.tree.2005.08.005
Barlow J, França F, Gardner TA, Hicks CC, Lennox GD, Berenguer E et al (2018) The future of hyperdiverse tropical ecosystems. Nature 559:517–526. https://doi.org/10.1038/s41586-018-0301-1
Benavides-Gordillo S, Farjalla VF, González AL, Romero GQ (2019) Changes in rainfall level and litter stoichiometry affect aquatic community and ecosystem processes in bromeliad phytotelmata. Freshw Biol 64:1357–1368. https://doi.org/10.1111/fwb.13310
Benzing DH (2000) Bromeliaceae: profile of an adaptive radiation. Cambridge University Press, Cambridge
Bernabé TN, de Omena PM, Santos VPD, de Siqueira VM, de Oliveira VM, Romero GQ (2018) Warming weakens facilitative interactions between decomposers and detritivores, and modifies freshwater ecosystem functioning. Glob Chang Biol 24:3170–3186. https://doi.org/10.1111/gcb.14109
Bosy JL, Reader RJ (1995) Mechanisms underlying the suppression of forb seedling emergence by grass (Poa pratensis) litter. Funct Ecol 9:635–639. https://doi.org/10.2307/2390155
Bruijnzeel LA (1991) Nutrient input-output budgets of tropical forest ecosystems: a review. J Trop Ecol 7:1–24. https://doi.org/10.1017/S0266467400005010
Cogliatti-Carvalho L, Rocha-Pessôa TC, Nunes-Freitas AF, Rocha CFD (2010) Volume de água armazenado no tanque de bromélias, em Restingas da costa brasileira. Acta Bot Bras 24:84–95. https://doi.org/10.1590/S0102-33062010000100009
Cooper TM, Frank JH, Cave RD (2014) Loss of phytotelmata due to an invasive bromeliad-eating weevil and its potential effects on faunal diversity and biogeochemical cycles. Acta Oecol 54:51–56. https://doi.org/10.1016/j.actao.2013.01.016
Dézerald O, Leroy C, Corbara B, Dejean A, Talaga S, Céréghino R (2018) Tank bromeliads sustain high secondary production in neotropical forests. Aquat Sci 80:1–12. https://doi.org/10.1007/s00027-018-0566-3
Di Virgilio G, Wardell-Johnson GW, Robinson TP, Temple-Smith D, Hesford J (2018) Characterising fine-scale variation in plant species richness and endemism across topographically complex, semi-arid landscapes. J Arid Environ 156:59–68. https://doi.org/10.1016/j.jaridenv.2018.04.005
Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167. https://doi.org/10.1146/annurev.energy.28.050302.105532
Farley RA, Fitter AH (1999) Temporal and spatial variation in soil resources in a deciduous woodland. J Ecol 87:688–696. https://doi.org/10.1046/j.1365-2745.1999.00390.x
Fish D (1983) Phytotelmata: flora and fauna. In: Frank JH, Lounibos LP (eds) Phytotelmata: terrestrial plants as hosts for aquatic insect communities. Plexus Publishing, Medford, pp 1–27
Fragoso JM, Silvius KM, Correa JA (2003) Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84:1998–2006. https://doi.org/10.1890/01-0621
Fujii K (2014) Soil acidification and adaptations of plants and microorganisms in Bornean tropical forests. Ecol Res 29:371–381. https://doi.org/10.1007/s11284-014-1144-3
García-Guzmán G, Benítez-Malvido J (2003) Effect of litter on the incidence of leaf-fungal pathogens and herbivory in seedlings of the tropical tree Nectandra ambigens. J Trop Ecol 19:171–177. https://doi.org/10.1017/S0266467403003195
Gonçalves-Souza T, Brescovit AD, de C. Rossa-Feres D, Romero GQ, (2010) Bromeliads as biodiversity amplifiers and habitat segregation of spider communities in a Neotropical rainforest. J Arachnol 38:270–279. https://doi.org/10.1636/P09-58.1
González-Zamora A, Arroyo-Rodríguez V, Oyama K, Sork V, Chapman CA, Stoner KE (2012) Sleeping sites and latrines of spider monkeys in continuous and fragmented rainforests: implications for seed dispersal and forest regeneration. PLoS ONE 7:e46852. https://doi.org/10.1371/journal.pone.0046852
Hayes PE, Guilherme Pereira C, Clode PL, Lambers H (2019) Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–777. https://doi.org/10.1111/nph.15447
Inselsbacher E, Cambui CA, Richter A, Stange CF, Mercier H, Wanek W (2007) Microbialactivities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea. New Phytol 175:311–320. https://doi.org/10.1111/j.1469-8137.2007.02098.x
Jucker T, Bongalov B, Burslem DF, Nilus R, Dalponte M, Lewis SL et al (2018) Topography shapes the structure, composition and function of tropical forest landscapes. Ecol Lett 21:989–1000. https://doi.org/10.1111/ele.12964
Junker RR, Kuppler J, Bathke AC, Schreyer ML, Trutschnig W (2016) Dynamic range boxes—a robust nonparametric approach to quantify size and overlap of n-dimensional hypervolumes. Methods Ecol Evol 7:1503–1513. https://doi.org/10.1111/2041-210X.12611
Ladino G, Ospina-Bautista F, Estévez Varón J, Jerabkova L, Kratina P (2019) Ecosystem services provided by bromeliad plants: a systematic review. Ecol Evol 9:7360–7372. https://doi.org/10.1002/ece3.5296
Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–1605. https://doi.org/10.1126/science.1256330
Laurance W (2009) Conserving the hottest of the hotspots. Biol Conserv 142:1137. https://doi.org/10.1016/j.biocon.2008.10.011
Leão TC, Fonseca CR, Peres CA, Tabarelli M (2014) Predicting extinction risk of Brazilian Atlantic Forest angiosperms. Conserv Biol 28:1349–1359. https://doi.org/10.1111/cobi.12286
Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257. https://doi.org/10.1038/nature08251
Lôbo D, Leão T, Melo FP, Santos AM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diver Distrib 17:287–296. https://doi.org/10.1111/j.1472-4642.2010.00739.x
Marino NAC, Guariento RD, Dib V, Azevedo FD, Farjalla VF (2011) Habitat size determine algae biomass in tank-bromeliads. Hydrobiologia 678:191–199. https://doi.org/10.1007/s10750-011-0848-4
Martinelli G, Vieira CM, Gonzalez M, Leitman P, Piratininga A, Costa AFD et al (2008) Bromeliaceae da Mata Atlântica brasileira: lista de espécies, distribuição e conservação. Rodriguésia 59:209–258. https://doi.org/10.1590/2175-7860200859114
Martins SC, Neto ES, de Cássia PM, Almeida DQ, de Camargo PB, do Carmo JB et al (2015) Soil texture and chemical characteristics along an elevation range in the coastal Atlantic Forest of Southeast Brazil. Geoderma Reg 5:106–116. https://doi.org/10.1016/j.geodrs.2015.04.005
Okin GS, Mahowald N, Chadwick OA, Artaxo P (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Glob Biogeochem Cycles 18:GB2005. https://doi.org/10.1029/2003GB002145
Pärtel M (2002) Local plant diversity patterns and evolutionary history at the regional scale. Ecology 83:2361–2366. https://doi.org/10.1890/0012-9658(2002)083[2361:LPDPAE]2.0.CO;2
Pearcy RW (2007) Responses of plants to heterogeneous light environments. In: Pugnaire FI, Valladares F (eds) Functional plant ecology, 2nd edn. CRC Press, Boca Raton, pp 213–258
Peters MK, Hemp A, Appelhans T, Behler C, Classen A, Detsch F et al (2016) Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level. Nat Commun 7:1–11. https://doi.org/10.1038/ncomms13736
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rocha CFD, Cogliatti-Carvalho L, Almeida DR, Freitas AFN (2000) Bromeliads: biodiversity amplifiers. J Bromel Soc 50:81–83
Rocha CFD, Bergallo HG, Van Sluys M, Alves MAS, Jamel CE (2007) The remnants of Restinga habitats in the Brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Braz J Biol 67:263–273. https://doi.org/10.1590/S1519-69842007000200011
Romero GQ, Gonçalves-Souza T, Vieira C, Koricheva J (2015) Ecosystem engineering effects on species diversity across ecosystems: a meta-analysis. Biol Rev 90:877–890. https://doi.org/10.1111/brv.12138
Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Ann Bot 90:517–524. https://doi.org/10.1093/aob/mcf189
Srivastava DS, Céréghino R, Trzcinski MK, MacDonald AAM, Marino NA, Mercado DA et al (2020) Ecological response to altered rainfall differs across the Neotropics. Ecology 101:e02984. https://doi.org/10.1002/ecy.2984
Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17:866–880. https://doi.org/10.1111/ele.12277
Tsuda ÉT, Castellani TT (2016) Vriesea friburgensis: a natural trap or a nurse plant in coastal sand dunes? Austral Ecol 41:273–281. https://doi.org/10.1111/aec.12308
Voigt CC, Borissov I, Kelm DH (2015) Bats fertilize roost trees. Biotropica 47:403–406. https://doi.org/10.1111/btp.12226
Wright SJ (2019) Plant responses to nutrient addition experiments conducted in tropical forests. Ecol Monogr 89:e01382. https://doi.org/10.1002/ecm.1382
Zotz G, Leja M, Aguilar-Cruz Y, Einzmann HJ (2020) How much water is in the tank? An allometric analysis with 205 bromeliad species. Flora 264:151557. https://doi.org/10.1016/j.flora.2020.151557