Abstract
The impacts of soil properties and fire regime on Neotropical savannas are well-known, but the importance of hydrological regime for plant species assembly has received less attention. Here, we assessed changes in diversity patterns of herbaceous and woody communities along a water table gradient in a fire-excluded Neotropical savanna. We found that increased waterlogging of soils was associated with declines in both herbaceous and woody species richness. Woody species richness decreased once the water table depth is less than 4 m and no woody species occurred once water table depth was less than 23 cm. Herbaceous communities remained species rich until the shallowest water table depth, where there is flooding at some point in the year, and even there, over a dozen species occurred. Woody species that occurred in areas with shallower water tables were a nested subset of those in areas with deeper water tables. In contrast, herbaceous communities showed turnover over the hydrological gradient, with distinct species specialized for different water table levels. However, we found that those specialists are restricted to few evolutionary lineages, evidenced by increased phylogenetic clustering over the water table gradient in herbaceous communities. We suggest that evolutionarily conserved hydrological niches define the herbaceous layer over the hydrological gradient, whereas only generalist woody species persist under high water tables. Our findings show that the effect of soil waterlogging differs between the herbaceous and woody layer of savannas, indicating that these communities will respond differently to shifts in the hydrological regime under future environmental change.
Similar content being viewed by others
References
Allen-Diaz BH (1991) Water table and plant species relationships in Sierra Nevada meadows. Am Midl Nat 126:30–43
Almeida-Neto M, Guimarães P, Guimarães PR, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x
Araya YN, Silvertown J, Gowing DJ, McConway KJ, Linder HP, Midgley G (2011) A fundamental, eco-hydrological basis for niche segregation in plant communities. New Phytol 189:253–258
Araya YN, Silvertown J, Gowing DJ, McConway KJ, Linder HP, Midgley G (2012) Do niche-structured plant communities exhibit phylogenetic conservatism? A test case in an endemic clade. J Ecol 100:1434–1439
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752
Batalha MA, Cianciaruso MV, Silva IA, Delitti WBC (2005) Hyperseasonal cerrado, a new Brazilian vegetation form. Braz J Biol 65:735–738
Bond WJ, Parr CL (2010) Beyond the forest edge: ecology, diversity and conservation of the grassy biomes. Biol Conserv 143:2395–2404. https://doi.org/10.1016/j.biocon.2009.12.012
Brockway DG, Lewis CE (1997) Long-term effects of dormant-season prescribed fire on plant community diversity, structure and productivity in a longleaf pine wiregrass ecosystem. For Ecol Manage 96:167–183. https://doi.org/10.1016/S0378-1127(96)03939-4
Bueno ML, Damasceno-Junior GA, Pott A, Pontara V, Seleme EP, Fava WS, Salomão AK, Ratter JA (2014) Structure of arboreal and herbaceous strata in a neotropical seasonally flooded monodominant savanna of Tabebuia aurea. Braz J Biol 74:325–337
Camargo OA, Moniz AC, Jorge JA, Valadares JAAS (2009) Métodos de Análise Química, Mineralógica e Física de Solos do Instituto Agronômico de Campinas
Casanova MT, Brock MA (2000) How do depth, duration and frequency of flooding influence the establishment of wetland plant communities? Plant Ecol 147:237–250
Cianciaruso MV, Antônio Batalha M, Aurélio da Silva I (2005) Seasonal variation of a hyperseasonal cerrado in Emas National Park, central Brazil. Flora Morphol Distrib Funct Ecol Plants 200:345–353. https://doi.org/10.1016/j.flora.2005.02.001
Cianciaruso MV, Silva IA, Batalha MA, Gaston KJ, Petchey OL (2012) The influence of fire on phylogenetic and functional structure of woody savannas: moving from species to individuals. Perspect Plant Ecol Evol Syst 14:205–216. https://doi.org/10.1016/j.ppees.2011.11.004
Clements FE (1936) Nature and structure of the climax. J Ecol 24:252–284
Coutinho LM (1978) O conceito do cerrado. Rev Bras de Bot 1:17–23
Dallas T (2014) metacom: an R package for the analysis of metacommunity structure. Ecography 37:402–405
de Castro EA, Kauffman JB (1998) Ecosystem structure in the Brazilian Cerrado: a vegetation gradient of aboveground biomass, root mass and consumption by fire. J Trop Ecol 14:263–283
de Paz AA, Ribeiro C, Azevedo AA, de Lima ER, da Silva Carmo FM (2017) Induced flooding as environmental filter for riparian tree species. Environ Exp Bot 139:31–38
Deil U (2005) A review on habitats, plant traits and vegetation of ephemeral wetlands—a global perspective. Phytocoenologia 35:533–706. https://doi.org/10.1127/0340-269X/2005/0035-0533
Desbarats AJ, Logan CE, Hinton MJ, Sharpe DR (2002) On the kriging of water table elevations using collateral information from a digital elevation model. J Hydrol 255:25–38. https://doi.org/10.1016/S0022-1694(01)00504-2
Dodd MB, Lauenroth WK, Welker JM (1998) Differential water resource use by herbaceous and woody plant life-forms in a shortgrass steppe community. Oecologia 117:504–512. https://doi.org/10.1007/s004420050686
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Dostál P, Fischer M, Chytrý M, Prati D (2016) No evidence for larger leaf trait plasticity in ecological generalists compared to specialists. J Biogeogr. https://doi.org/10.1111/jbi.12881
Durigan G, Ratter JA (2016) The need for a consistent fire policy for Cerrado conservation. J Appl Ecol 53:11–15
Durigan G, Siqueira MFd, Franco GADC (2007) Threats to the Cerrado remnants of the state of São Paulo, Brazil. Sci Agric 64:355–363
Dwire KA, Kauffman JB, Baham JE (2006) Plant species distribution in relation to water-table depth and soil redox potential in montane riparian meadows. Wetlands 26:131–146
Eden M (1970) Savanna vegetation in the northern Rupununi, Guyana. J Trop Geogr 30:17–28
Esquivel-Muelbert A, Baker TR, Dexter KG, Lewis SL, ter Steege H, Lopez-Gonzalez G, Monteagudo Mendoza A, Brienen R, Feldpausch TR, Pitman N, Alonso A (2016) Seasonal drought limits tree species across the neotropics. Ecography 40:618–629. https://doi.org/10.1111/ecog.01904
Fine PVA, Kembel SW (2011) Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34:552–565. https://doi.org/10.1111/j.1600-0587.2010.06548.x
Francesco Ficetola G, Denoël M (2009) Ecological thresholds: an assessment of methods to identify abrupt changes in species–habitat relationships. Ecography 32:1075–1084. https://doi.org/10.1111/j.1600-0587.2009.05571.x
Garssen AG, Baattrup-Pedersen A, Voesenek LACJ, Verhoeven JTA, Soons MB (2015) Riparian plant community responses to increased flooding: a meta-analysis. Glob Change Biol 21:2881–2890. https://doi.org/10.1111/gcb.12921
Garssen AG, Baattrup-Pedersen A, Riis T, Raven BM, Hoffman CC, Verhoeven JT, Soons MB (2017) Effects of increased flooding on riparian vegetation: field experiments simulating climate change along five European lowland streams. Glob Change Biol 23:3052–3063
Gastauer M, Meira-Neto JAA (2017) Updated angiosperm family tree for analyzing phylogenetic diversity and community structure. Acta Bot Brasilica 31:191–198
Grime JP (1988) The CSR model of primary plant strategies—origins, implications and tests. Plant evolutionary biology. Springer, New York, pp 371–393
Hamilton SK, Sippel SJ, Melack JM (2004) Seasonal inundation patterns in two large savanna floodplains of South America: the Llanos de Moxos (Bolivia) and the Llanos del Orinoco (Venezuela and Colombia). Hydrol Process 18:2103–2116. https://doi.org/10.1002/hyp.5559
Hempson GP, Archibald S, Bond WJ (2015) A continent-wide assessment of the form and intensity of large mammal herbivory in Africa. Science 350:1056–1061
Honorio Coronado EN, Dexter KG, Pennington RT, Chave J, Lewis SL, Alexiades MN, Alvarez E, Alves de Oliveira A, Amaral IL, Araujo-Murakami A, Arets EJ (2015) Phylogenetic diversity of Amazonian tree communities. Divers Distrib 21:1295–1307
IFSP (2018) Dados meterologicos—Estação Ecologica de Itirapina. Instituto Florestal de São Paulo. http://www.iflorestal.sp.gov.br/Itirapina/dados_metereologicos.html
Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Killeen TJ, Hinz PN (1992) Grasses of the Precambrian Shield region in eastern lowland Bolivia. I. Habitat preferences. J Tropical Ecol 8(4):389–407
Kirkman LK, Mitchell RJ, Helton RC, Drew MB (2001) Productivity and species richness across an environmental gradient in a fire-dependent ecosystem. Am J Bot 88:2119–2128
Kolb RM, Joly CA (2009) Flooding tolerance of Tabebuia cassinoides: metabolic, morphological and growth responses. Flora Morphol Distrib Funct Ecol Plants 204:528–535. https://doi.org/10.1016/j.flora.2008.07.004
Kozlowski T (1984) Plant responses to flooding of soil. Bioscience 34:162–167
Kozlowski T (1997) Responses of woody plants to flooding and salinity. Tree Physiol 17:490
Kubota Y, Hirao T, S-j Fujii, Shiono T, Kusumoto B (2014) Beta diversity of woody plants in the Japanese archipelago: the roles of geohistorical and ecological processes. J Biogeogr 41:1267–1276. https://doi.org/10.1111/jbi.12290
Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–1605
Lehmann CE, Anderson TM, Sankaran M, Higgins SI, Archibald S, Hoffmann WA, Hanan NP, Williams RJ, Fensham RJ, Felfili J, Hutley LB (2014) Savanna vegetation-fire-climate relationships differ among continents. Science 343:548–552. https://doi.org/10.1126/science.1247355
Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: elements of meta-community structure. Oikos 97:237–250. https://doi.org/10.1034/j.1600-0706.2002.970210.x
Leite MB, Xavier RO, Oliveira PTS, Silva FKG, Matos DMS (2018) Groundwater depth as a constraint on the woody cover in a Neotropical Savanna. Plant Soil 426:1–15
Lewthwaite JMM, Debinski DM, Kerr JT (2017) High community turnover and dispersal limitation relative to rapid climate change. Glob Ecol Biogeogr 26:459–471. https://doi.org/10.1111/geb.12553
Lite SJ, Stromberg JC (2005) Surface water and ground-water thresholds for maintaining Populus-Salix forests, San Pedro River, Arizona. Biol Conserv 125:153–167
Lloyd J, Bird MI, Vellen L, Miranda AC, Veenendaal EM, Djagbletey G, Miranda HS, Cook G, Farquhar GD (2008) Contributions of woody and herbaceous vegetation to tropical savanna ecosystem productivity: a quasi-global estimate†. Tree Physiol 28:451–468. https://doi.org/10.1093/treephys/28.3.451
McGinness HM, Arthur AD, Davies M (2018) Flood regimes driving vegetation and bird community transitions in semiarid floodplain woodlands. Ecohydrology 11:e1954. https://doi.org/10.1002/eco.1954
Mendonça RC, Felfili JM, Walter BM, Silva M, Rezende A, Filgueiras TS, Nogueira PE (1998) Flora vascular do cerrado. In: Sano SM, Almeida SP (eds) Cerrado: ambiente e flora. Embrapa, Planaltina, pp 289–556
Mendonça RC, Felfili JM, Walter BM, Silva-Júnior MD, Rezende AV, Filgueiras TD, Nogueira PE, Fagg CW (2008) Flora vascular do bioma cerrado: checklist com 12.356 espécies. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora. Embrapa Cerrados, Planaltina, pp 421–1279
Mommer L, Lenssen JPM, Huber H, Visser EJW, Kroon HD (2006) Ecophysiological determinants of plant performance under flooding: a comparative study of seven plant families. J Ecol 94:1117–1129. https://doi.org/10.1111/j.1365-2745.2006.01175.x
Moore R (1939) Water conduction from shallow water tables. Hilgardia 12:383–426
Moreira AG (2000) Effects of fire protection on savanna structure in Central Brazil. J Biogeogr 27:1021–1029. https://doi.org/10.1046/j.1365-2699.2000.00422.x
Morgan C, Stolt M (2004) A comparison of several approaches to monitor water-table fluctuations. Soil Sci Soc Am J 68:562–566
Moro MF, Silva IA, Araújo FSd, Nic Lughadha E, Meagher TR, Martins FR (2015) The role of edaphic environment and climate in structuring phylogenetic pattern in seasonally dry tropical plant communities. PLoS One 10:e0119166. https://doi.org/10.1371/journal.pone.0119166
Moulatlet GM, Costa FRC, Rennó CD, Emilio T, Schietti J (2014) Local hydrological conditions explain floristic composition in Lowland Amazonian forests. Biotropica 46:395–403. https://doi.org/10.1111/btp.12117
Munhoz C, Felfili J (2006) Floristics of the herbaceous and subshrub layer of a moist grassland in the Cerrado biosphere reserve (Alto Paraíso de Goiás), Brazil. Edinb J Bot 63:343–354
Oksanen J, Blanchet FG, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5-4. https://CRAN.R-project.org/package=vegan
Oliveira RS, Bezerra L, Davidson EA, Pinto F, Klink CA, Nepstad DC, Moreira A (2005) Deep root function in soil water dynamics in cerrado savannas of central Brazil. Funct Ecol 19:574–581. https://doi.org/10.1111/j.1365-2435.2005.01003.x
Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312. https://doi.org/10.1016/S0098-8472(01)00107-1
Pyke CR, Condit R, Aguilar S, Lao S (2001) Floristic composition across a climatic gradient in a neotropical lowland forest. J Veg Sci 12:553–566. https://doi.org/10.2307/3237007
R Core Team (2019) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Rawitscher F (1948) The water economy of the vegetation of the `Campos Cerrados’ in Southern Brazil. J Ecol 36:237–268. https://doi.org/10.2307/2256669
Rezende VL, Dexter KG, Pennington RT, Oliveira-Filho AT (2017) Geographical variation in the evolutionary diversity of tree communities across southern South America. J Biogeogr 44:2365–2375. https://doi.org/10.1111/jbi.13013
Munhoz CBR, Felfili JM (2007) Florística do estrato herbáceo-subarbustivo de um campo limpo úmido em Brasília, Brasil. Biota Neotropica 7:205–215
Rossatto DR, Kolb RM (2010) Gochnatia polymorpha (Less.) Cabrera (Asteraceae) changes in leaf structure due to differences in light and edaphic conditions. Acta Bot Bras 24:605–612
Sankaran M, Hanan NP, Scholes RJ, Ratnam J, Augustine DJ, Cade BS, Gignoux J, Higgins SI, Le Roux X, Ludwig F, Ardo J (2005) Determinants of woody cover in African savannas. Nature 438:846
Sarmiento G (1984) The ecology of Neotropical Savannas. Harvard University Press, Cambridge
Sarmiento G, Pinillos M (2001) Patterns and processes in a seasonally flooded tropical plain: the Apure Llanos, Venezuela. J Biogeogr 28:985–996. https://doi.org/10.1046/j.1365-2699.2001.00601.x
Sarmiento G, Pinillos M, Silva MP, Acevedo D (2004) Effects of soil water regime and grazing on vegetation diversity and production in a hyperseasonal savanna in the Apure Llanos, Venezuela. J Trop Ecol 20:209–220
Scholes R, Dowty P, Caylor K, Parsons DAB, Frost PGH, Shugart H (2002) Trends in savanna structure and composition along an aridity gradient in the Kalahari. J Veg Sci 13:419–428
Shafroth PB, Stromberg JC, Patten DT (2000) Woody riparian vegetation response to different alluvial water table regimes. West N Am Nat 60:66–76
Silva IA, Batalha MA (2010) Phylogenetic structure of Brazilian savannas under different fire regimes. J Veg Sci 21:1003–1013. https://doi.org/10.1111/j.1654-1103.2010.01208.x
Silvertown J, Dodd ME, Gowing DJG, Mountford JO (1999) Hydrologically defined niches reveal a basis for species richness in plant communities. Nature 400:61. https://doi.org/10.1038/21877
Silvertown J, Araya Y, Gowing D, Cornwell W (2015) Hydrological niches in terrestrial plant communities: a review. J Ecol 103:93–108. https://doi.org/10.1111/1365-2745.12332
Somavilla NS, Graciano-Ribeiro D (2011) Análise comparativa da anatomia foliar de Melastomataceae em ambiente de vereda e cerrado sensu stricto. Acta Bot Bras 25:764–775
Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of Savanna and forest as alternative biome states. Science 334:230–232. https://doi.org/10.1126/science.1210465
Stevens N, Lehmann CER, Murphy BP, Durigan G (2016) Savanna woody encroachment is widespread across three continents. Global Change Biol. https://doi.org/10.1111/gcb.13409
Stevenson PR, Aldana AM, Cárdenas S, Negret PJ (2018) Flooding and soil composition determine beta diversity of lowland forests in Northern South America. Biotropica 50:568–577. https://doi.org/10.1111/btp.12541
Tanentzap AJ, Lee WG (2016) Evolutionary conservatism explains increasing relatedness of plant communities along a flooding gradient. New Phytol. https://doi.org/10.1111/nph.14167
Tannus JLS, Assis MA (2004) Composição de espécies vasculares de campo sujo e campo úmido em área de cerrado, Itirapina—SP, Brasil. Braz J Bot 27:489–506
Targhetta N, Kesselmeier J, Wittmann F (2015) Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobot 50:185–205. https://doi.org/10.1007/s12224-015-9225-9
Tilman D (1985) The resource-ratio hypothesis of plant succession. Am Nat 125:827–852. https://doi.org/10.1086/284382
Ulrich W, Almeida-Neto M, Gotelli NJ (2009) A consumer’s guide to nestedness analysis. Oikos 118:3–17. https://doi.org/10.1111/j.1600-0706.2008.17053.x
Villalobos-Vega R, Salazar A, Miralles-Wilhelm F, Haridasan M, Franco AC, Goldstein G (2014) Do groundwater dynamics drive spatial patterns of tree density and diversity in Neotropical savannas? J Veg Sci 25:1465–1473. https://doi.org/10.1111/jvs.12194
Wakindiki I, Ben-Hur M (2002) Soil mineralogy and texture effects on crust micromorphology, infiltration, and erosion. Soil Sci Soc Am J 66:897–905
Walter H (1979) Vegetation of the earth and ecological systems of the geo-biosphere, 2nd edn. Springer, Berlin, Heidelberg, New York
Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Resour 5:181–183
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100
Wegner LH (2010) Oxigen trasport in waterlogged plants. In: Mancuso SCS (ed) Waterlogging signalling and tolerance in plants. Springer, Berlin
Wei X, Liu M, Wang S, Jiang M (2018) Seed morphological traits and seed element concentrations of an endangered tree species displayed contrasting responses to waterlogging induced by extreme precipitation. Flora 246–247:19–25. https://doi.org/10.1016/j.flora.2018.07.001
Whittaker RH (1956) Vegetation of the Great Smoky Mountains. Ecol Monogr 26:1–80. https://doi.org/10.2307/1943577
Wickham H (2010) ggplot2: elegant graphics for data analysis. J Stat Softw 35:65–88
Wilke CO (2019) Cowplot: streamlined plot theme and plot annotations for 'ggplot2'. R package version 0.9.4. https://CRAN.R-project.org/package=cowplot
Wood S (2006) Generalized additive models: an introduction with R. CRC Press, Boca Raton
Xavier RdO, Leite MB, da Silva-Matos DM (2016) Stress responses of native and exotic grasses in a Neotropical savanna predict impacts of global change on invasion spread. Aust Ecol. https://doi.org/10.1111/aec.12475
Xavier RO, Leite MB, da Silva-Matos DM (2017) Stress responses of native and exotic grasses in a Neotropical savanna predict impacts of global change on invasion spread. Aust Ecol 42:562–576
Yan Y, Yang X, Tang Z (2013) Patterns of species diversity and phylogenetic structure of vascular plants on the Qinghai-Tibetan Plateau. Ecol Evol 3:4584–4595. https://doi.org/10.1002/ece3.847
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin
Acknowledgements
We are thankful to the Coordination for the Improvement of Higher Education Personnel (CAPES) for the funding granted to R.O. Xavier and M.B. Leite and to the State of São Paulo Research Foundation (FAPESP) for the scholarship granted to R.O. Xavier (Grant 2011/21019-6). K.G. Dexter was supported be a Leverhulme International Academic Fellowship during the time this work was completed. We also thank the São Paulo Forestry Institute for the research permit and to the Itirapina Ecological Station staff for logistical assistance, and the Royal Botanical Garden Edinburgh for providing full access to its collection. We thank A. Magurran for her initial contribution on the conceptual direction of the study manuscript. J. Veldman and an anonymous reviewer made valuable suggestions to improve later versions of the manuscript.
Author information
Authors and Affiliations
Contributions
ROX, MBL and DMS conceived the ideas and designed the methodology; ROX and MBL collected the data; ROX and KD analysed the data; ROX and KD led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Additional information
Communicated by Brian J. Wilsey.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Oliveira Xavier, R., Leite, M.B., Dexter, K. et al. Differential effects of soil waterlogging on herbaceous and woody plant communities in a Neotropical savanna. Oecologia 190, 471–483 (2019). https://doi.org/10.1007/s00442-019-04423-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04423-y