Waterlogging as an environmental filter to tree recruitment in tropical wet grasslands
Jonathan Wesley Ferreira Ribeiro A B * , Rafael Reis Gonçalo B and Rosana Marta Kolb A BA Instituto de Biociências, Universidade Estadual Paulista, 13506-900 Rio Claro, SP, Brazil.
B Faculdade de Ciências e Letras, Universidade Estadual Paulista, 19806-900 Assis, SP, Brazil.
Australian Journal of Botany 69(8) 543-553 https://doi.org/10.1071/BT20173
Submitted: 30 December 2020 Accepted: 21 July 2021 Published: 14 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Wet grasslands from the Brazilian Savanna (Cerrado) are open-canopy vegetation dominated by subshrubs and herbaceous plants. Although they frequently occur between gallery forests and savannas, tree species are rarely observed colonising these grasslands. Here, seed germination and seedling development of Cerrado trees under waterlogging conditions were evaluated in order to elucidate how soil waterlogging constrains tree regeneration in tropical wet grasslands. We used seeds of 11 representative Cerrado tree species that have different requirements for soil moisture (non-flooded v. flooded environments). Short periods (15 days) of waterlogging drastically decreased or inhibited germination and seedling development in four species, whereas long periods (30–45 days) of waterlogging reduced or inhibited germination and seedling development in 6 of the 11 species. As expected, we found fewer waterlogging-resistant seeds associated with those species from non-flooded environments. By contrast, more waterlogging-resistant seeds were associated with species that eventually or typically occur in flooded environments. Our results suggest that soil waterlogging is an important environmental filter constraining tree recruitment in tropical wet grasslands. However, some species can overcome this environmental filter by possessing waterlogging-resistant seeds or avoid it by establishing in less waterlogged locations.
Keywords: Brazilian grassland, Cerrado, flooding, flood tolerance, seasonal waterlogging, seed germination, seedling development, tropical savannas, vegetation mosaics.
References
Abreu RCR, Hoffmann WA, Vasconcelos HL, Pilon NA, Rossatto DR, Durigan G (2017) The biodiversity cost of carbon sequestration in tropical savanna. Science Advances 3, e1701284| The biodiversity cost of carbon sequestration in tropical savanna.Crossref | GoogleScholarGoogle Scholar | 28875172PubMed |
Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.
| Köppen’s climate classification map for Brazil.Crossref | GoogleScholarGoogle Scholar |
Araújo-Neto MD, Furley PA, Haridasan M, Johnson CE (1986) The murundus of the cerrado region of Central Brazil. Journal of Tropical Ecology 2, 17–35.
| The murundus of the cerrado region of Central Brazil.Crossref | GoogleScholarGoogle Scholar |
Archibald S, Bond WJ (2003) Growing tall vs growing wide: tree architecture and allometry of Acacia karroo in forest, savanna, and arid environments. Oikos 102, 3–14.
| Growing tall vs growing wide: tree architecture and allometry of Acacia karroo in forest, savanna, and arid environments.Crossref | GoogleScholarGoogle Scholar |
Assis ACC, Coelho RM, Pinheiro ES, Durigan G (2011) Water availability determines physiognomic gradient in an area of low-fertility soils under Cerrado vegetation. Plant Ecology 212, 1135–1147.
| Water availability determines physiognomic gradient in an area of low-fertility soils under Cerrado vegetation.Crossref | GoogleScholarGoogle Scholar |
Bao F, Elsey-Quirk T, Assis MA, Pott A (2018) Seed bank of seasonally flooded grassland: experimental simulation of flood and post-flood. Aquatic Ecology 52, 93–105.
| Seed bank of seasonally flooded grassland: experimental simulation of flood and post-flood.Crossref | GoogleScholarGoogle Scholar |
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Bond WJ (2008) What limits trees in C4 grasslands and savannas? Annual Review of Ecology, Evolution, and Systematics 39, 641–659.
| What limits trees in C4 grasslands and savannas?Crossref | GoogleScholarGoogle Scholar |
Bond WJ, Parr CL (2010) Beyond the forest edge: ecology, diversity and conservation of the grassy biomes. Biological Conservation 143, 2395–2404.
| Beyond the forest edge: ecology, diversity and conservation of the grassy biomes.Crossref | GoogleScholarGoogle Scholar |
Bond WJ, Woodward FI, Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytologist 165, 525–538.
| The global distribution of ecosystems in a world without fire.Crossref | GoogleScholarGoogle Scholar |
Carlos NA, Rossatto DR (2017) Leaf traits combinations may explain the occurrence of savanna herbaceous species along a gradient of tree encroachment. Theoretical and Experimental Plant Physiology 29, 155–163.
| Leaf traits combinations may explain the occurrence of savanna herbaceous species along a gradient of tree encroachment.Crossref | GoogleScholarGoogle Scholar |
Colli-Silva M (2020) Guazuma in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB9065 [Verified 03 June 2021]
Crawford RMM (1992) Oxygen availability as an ecological limit to plant distribution. Advances in Ecological Research 23, 93–185.
| Oxygen availability as an ecological limit to plant distribution.Crossref | GoogleScholarGoogle Scholar |
Donohue K, Casas RR, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annuals Reviews of Ecology, Evolution, and Systematics 41, 293–319.
| Germination, postgermination adaptation, and species ecological ranges.Crossref | GoogleScholarGoogle Scholar |
Durigan D, Ratter WA (2006) Successional changes in cerrado and cerrado/forest ecotonal vegetation in western São Paulo State, Brazil, 1962–2000. Edinburgh Journal of Botany 63, 119–130.
| Successional changes in cerrado and cerrado/forest ecotonal vegetation in western São Paulo State, Brazil, 1962–2000.Crossref | GoogleScholarGoogle Scholar |
Durigan G, Fligliolia MB, Kawabata M, Garrido MAO, Baitelo JB (1997) ‘Sementes e mudas de árvores tropicais.’ (Páginas e Letras: São Paulo, Brazil)
Durigan G, Bacic MC, Franco GADC, Siqueira MF (1999) Inventário florístico do cerrado na Estação Ecológica de Assis, SP. Hoehnea 26, 149–172.
Durigan G, Siqueira MF, Franco GADC (2007) Threats to the Cerrado remnants of the state of São Paulo, Brazil. Scientia Agricola 64, 355–363.
| Threats to the Cerrado remnants of the state of São Paulo, Brazil.Crossref | GoogleScholarGoogle Scholar |
Fraaije RGA, ter Braak CJF, Verduyn B, Breeman LBS, Verhoeven JTA, Soons MB (2015) Early plant recruitment stages set the template for the development of vegetation patterns along a hydrological gradient. Functional Ecology 29, 971–980.
| Early plant recruitment stages set the template for the development of vegetation patterns along a hydrological gradient.Crossref | GoogleScholarGoogle Scholar |
Hoffmann WA, Orthen B, Franco AC (2004) Constraints to seedling success of savanna and forest trees across the savanna-forest boundary. Oecologia 140, 252–260.
| Constraints to seedling success of savanna and forest trees across the savanna-forest boundary.Crossref | GoogleScholarGoogle Scholar | 15148603PubMed |
Hoffmann WA, Adasme R, Haridasan M, Carvalho MT, Geiger EL, Pereira MAB, Franco AC (2009) Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil. Ecology 90, 1326–1337.
| Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil.Crossref | GoogleScholarGoogle Scholar | 19537552PubMed |
Honda EA, Durigan G (2016) Woody encroachment and its consequences on hydrological processes in the savannah. Philosophical Transactions of the Royal Society B: Biological Sciences 371, 20150313
| Woody encroachment and its consequences on hydrological processes in the savannah.Crossref | GoogleScholarGoogle Scholar |
Juhász CEP, Cursi PR, Cooper M, Oliveira TC, Rodrigues RR (2006) Dinâmica físico-hídrica de uma topossequência de solos sob savana florestada (cerradão) em Assis, SP. Revista Brasileira de Ciência do Solo 30, 401–412.
| Dinâmica físico-hídrica de uma topossequência de solos sob savana florestada (cerradão) em Assis, SP.Crossref | GoogleScholarGoogle Scholar |
Keddy P (1992) A pragmatic approach to functional ecology. Functional Ecology 6, 621–626.
| A pragmatic approach to functional ecology.Crossref | GoogleScholarGoogle Scholar |
Kissmann C, Veiga EB, Eichemberg MT, Habermann G (2014) Morphological effects of flooding on Styrax pohlii and the dynamics of physiological responses during flooding and post-flooding conditions. Aquatic Botany 119, 7–14.
| Morphological effects of flooding on Styrax pohlii and the dynamics of physiological responses during flooding and post-flooding conditions.Crossref | GoogleScholarGoogle Scholar |
Kolb RM, Joly CA (2010) Germination and anaerobic metabolism of seeds of Tabebuia cassinoides (Lam.) DC subjected to flooding and anoxia. Flora – Morphology, Distribution, Functional Ecology of Plants 205, 112–117.
| Germination and anaerobic metabolism of seeds of Tabebuia cassinoides (Lam.) DC subjected to flooding and anoxia.Crossref | GoogleScholarGoogle Scholar |
Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiology 17, 490–490.
| Responses of woody plants to flooding and salinity.Crossref | GoogleScholarGoogle Scholar |
Leite MB, Xavier RO, Oliveira PTS, Silva FKG, Silva Matos DM (2018) Groundwater depth as a constraint on the woody cover in a Neotropical Savanna. Plant and Soil 426, 1–15.
| Groundwater depth as a constraint on the woody cover in a Neotropical Savanna.Crossref | GoogleScholarGoogle Scholar |
Lohmann LG (2020) Handroanthus in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB114085 [Verified 03 June 2021]
Lopez OR (2001) Seed flotation and postflooding germination in tropical terra firme and seasonally flooded forest species. Functional Ecology 15, 763–771.
| Seed flotation and postflooding germination in tropical terra firme and seasonally flooded forest species.Crossref | GoogleScholarGoogle Scholar | 34638148PubMed |
Marques MCM, Joly CA (2000) Germinação e crescimento de Calophyllum brasiliense (Clusiaceae), uma espécie típica de florestas inundadas. Acta Botanica Brasilica 14, 113–120.
| Germinação e crescimento de Calophyllum brasiliense (Clusiaceae), uma espécie típica de florestas inundadas.Crossref | GoogleScholarGoogle Scholar |
Mendonça RC, Felfili JM, Walter BMT, Silva Júnior MC, Rezende AV, Filgueiras TS, Nogueira PE, Fagg CW (2008) Flora Vascular do Bioma Cerrado: Checklist com 12.356 espécies. In ‘Cerrado: Ecologia e Flora’. (Eds SM Sano, SP Almeida, JF Ribeiro) pp. 423–442. (Embrapa Informação Tecnológica: Brasília, Brazil)
Milberg P, Andersson L, Thompson K (2000) Large-seeded species are less dependent on light for germination than small-seeded ones. Seed Science Research 10, 99–104.
| Large-seeded species are less dependent on light for germination than small-seeded ones.Crossref | GoogleScholarGoogle Scholar |
Oliveira AKM, Gualtieri SCJ (2017) Trocas gasosas e grau de tolerância ao estresse hídrico induzido em plantas jovens de Tabebuia aurea (paratudo) submetidas a alagamento. Ciência Florestal 27, 181–191.
| Trocas gasosas e grau de tolerância ao estresse hídrico induzido em plantas jovens de Tabebuia aurea (paratudo) submetidas a alagamento.Crossref | GoogleScholarGoogle Scholar |
Oliveira PC, Parolin P, Borghetti F (2019) Can germination explain the distribution of tree species in a savanna wetland? Austral Ecology 44, 1373–1383.
| Can germination explain the distribution of tree species in a savanna wetland?Crossref | GoogleScholarGoogle Scholar |
Oliveira-Filho AT, Ratter JA (1995) A study of the origin of central Brazilian forests by the analysis of plant species distribution patterns. Edinburgh Journal of Botany 52, 141–194.
| A study of the origin of central Brazilian forests by the analysis of plant species distribution patterns.Crossref | GoogleScholarGoogle Scholar |
Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In ‘The Cerrados of Brazil: ecology and natural history of a neotropical savanna’. (Eds PS Oliveira, RJ Marquis) pp. 91–120. (Columbia University Press: New York, NY, USA)
Otte ML (2001) What is stress to a wetland plant? Environmental and Experimental Botany 46, 195–202.
| What is stress to a wetland plant?Crossref | GoogleScholarGoogle Scholar |
Parent C, Capelli N, Berger A, Crèvecoeur M, Dat J (2008) An overview of plant responses to soil waterlogging. Plant Stress 2, 20–27.
Paz AA, Ribeiro C, Azevedo AA, Lima ER, Carmo FMS (2017) Induced flooding as environmental filter for riparian tree species. Environmental and Experimental Botany 139, 31–38.
| Induced flooding as environmental filter for riparian tree species.Crossref | GoogleScholarGoogle Scholar |
Pérez-Ramos IM, Marañón T (2009) Effects of waterlogging on seed germination of three Mediterranean oak species: ecological implications. Acta Oecologica 35, 422–428.
| Effects of waterlogging on seed germination of three Mediterranean oak species: ecological implications.Crossref | GoogleScholarGoogle Scholar |
Pinheiro LFS, Kolb RM, Rossatto DR (2016) Changes in irradiance and soil properties explain why typical non-arboreal savanna species disappear under tree encroachment. Australian Journal of Botany 64, 333–341.
| Changes in irradiance and soil properties explain why typical non-arboreal savanna species disappear under tree encroachment.Crossref | GoogleScholarGoogle Scholar |
Pinheiro LFS, Kolb RM, Rossatto DR (2018) Leaf anatomical traits of non-arboreal savanna species along a gradient of tree encroachment. Acta Botanica Brasilica 32, 28–36.
| Leaf anatomical traits of non-arboreal savanna species along a gradient of tree encroachment.Crossref | GoogleScholarGoogle Scholar |
Pires HRA, Franco AC, Piedade MTF, Scudeller VV, Kruijt B, Ferreira CS (2018) Flood tolerance in two tree species that inhabit both the Amazonian floodplain and the dry Cerrado savanna of Brazil. AoB PLANTS 10, 1–15.
| Flood tolerance in two tree species that inhabit both the Amazonian floodplain and the dry Cerrado savanna of Brazil.Crossref | GoogleScholarGoogle Scholar |
Quinn GP, Keough MJ (2002) ‘Experimental design and data analysis for biologists.’ (Cambridge University Press: Cambridge, UK)
Ratter JA, Bridgewater S, Ribeiro JF (2003) Analysis of the floristic composition of the Brazilian Cerrado Vegetation. III. Comparison of the woody Vegetation of 376 areas. Edinburgh Journal of Botany 60, 57–109.
| Analysis of the floristic composition of the Brazilian Cerrado Vegetation. III. Comparison of the woody Vegetation of 376 areas.Crossref | GoogleScholarGoogle Scholar |
Ribeiro JF, Walter BMT (2008) Fitofisionomias do Bioma Cerrado. In ‘Cerrado: Ambiente e Flora’. (Eds SM Sano, SP Almeida) pp. 151–212. (EMBRAPA-CPAC: Brasília, Brazil)
Ribeiro JWF, Kolb RM (2016) Distinct germination responses may contribute to the distribution pattern of two Moquiniastrum species in different phytophysiognomies from the Brazilian savanna. Flora 223, 159–166.
| Distinct germination responses may contribute to the distribution pattern of two Moquiniastrum species in different phytophysiognomies from the Brazilian savanna.Crossref | GoogleScholarGoogle Scholar |
Ribeiro JWF, Pilon NAL, Rossatto DR, Durigan G, Kolb RM (2021) The distinct roles of water table depth and soil properties in controlling alternative woodland–grassland states in the Cerrado. Oecologia 195, 641–653.
| The distinct roles of water table depth and soil properties in controlling alternative woodland–grassland states in the Cerrado.Crossref | GoogleScholarGoogle Scholar | 33619596PubMed |
Rodrigues JAM, Viola MR, Alvarenga LA, de Mello CR, Chou SC, Oliveira VA, Uddameri V, Morais MAV (2020) Climate change impacts under representative concentration pathway scenarios on streamflow and droughts of basins in the Brazilian Cerrado biome. International Journal of Climatology 40, 2511–2526.
| Climate change impacts under representative concentration pathway scenarios on streamflow and droughts of basins in the Brazilian Cerrado biome.Crossref | GoogleScholarGoogle Scholar |
Romão GO, Cabral A, Fritsch PW, Santos FBD (2020) Styracaceae in Flora do Brasil 2020, Jardim Botânico do Rio de Janeiro. Available at http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB21256 [Verified 03 June 2021]
Rossatto DR, Hoffmann WA, Franco AC (2009) Differences in growth patterns between co-occurring forest and savanna trees affect the forest-savanna boundary. Functional Ecology 23, 689–698.
| Differences in growth patterns between co-occurring forest and savanna trees affect the forest-savanna boundary.Crossref | GoogleScholarGoogle Scholar |
Sancho G, Roque N (2020) Moquiniastrum Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. Available at http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB130869 [Verified 03 June 2021]
Secretaria do Meio Ambiente (2010) ‘Plano de manejo da estação ecológica de Assis’. (Secretaria do Meio Ambiente: São Paulo, Brazil). Available at https://smastr16.blob.core.windows.net/iflorestal/2013/03/Plano_de_Manejo_EEc_Assis.pdf [Verified 17 April 2020]
Souza GF, Almeida RF, Bijos NR, Fagg CW, Munhoz CBR (2021) Herbaceous-shrub species composition, diversity and soil attributes in moist grassland, shrub grassland and savanna in Central Brazil. Brazilian Journal of Botany 44, 227–238.
| Herbaceous-shrub species composition, diversity and soil attributes in moist grassland, shrub grassland and savanna in Central Brazil.Crossref | GoogleScholarGoogle Scholar |
Teixeira AP, Assis MA, Luize BG (2011) Vegetation and environmental heterogeneity relationships in a Neotropical swamp forest in southeastern Brazil (Itirapina, SP). Aquatic Botany 94, 17–23.
| Vegetation and environmental heterogeneity relationships in a Neotropical swamp forest in southeastern Brazil (Itirapina, SP).Crossref | GoogleScholarGoogle Scholar |
Urquhart GR (2004) Flood-tolerance and flood-escape mechanisms for seeds and seedlings of common swamp trees of Central America. Tropical Ecology 45, 197–208.
van der Valk AG (1981) Succession in wetlands: a Gleasonian approach. Ecology 62, 688–696.
| Succession in wetlands: a Gleasonian approach.Crossref | GoogleScholarGoogle Scholar |
van der Valk AG, Bremholm TL, Gordon E (1999) The restoration of sedge meadows: seed viability, seed germination requirements, and seedling growth of Carex species. Wetlands 19, 756–764.
| The restoration of sedge meadows: seed viability, seed germination requirements, and seedling growth of Carex species.Crossref | GoogleScholarGoogle Scholar |
Veldman JW, Buisson E, Durigan G, Fernandes GW, Le Stradic S, Mahy G, et al. (2015) Toward an old-growth concept for grasslands, savannas, and woodlands. Frontiers in Ecology and the Environment 13, 154–162.
| Toward an old-growth concept for grasslands, savannas, and woodlands.Crossref | GoogleScholarGoogle Scholar |
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? Journal of Vegetation Science 25, 1465–1473.
| Do groundwater dynamics drive spatial patterns of tree density and diversity in Neotropical savannas?Crossref | GoogleScholarGoogle Scholar |
Wittmann F, Householder E, Piedade MTF, Assis RL, Schöngart J, Parolin P, Junk WJ (2013) Habitat specifity, endemism and the neotropical distribution of Amazonian white-water floodplain trees. Ecography 36, 690–707.
| Habitat specifity, endemism and the neotropical distribution of Amazonian white-water floodplain trees.Crossref | GoogleScholarGoogle Scholar |
Xavier RO, Leite MB, Dexter K, Matos DMS (2019) Differential effects of soil waterlogging on herbaceous and woody plant communities in a Neotropical savanna. Oecologia 190, 471–483.
| Differential effects of soil waterlogging on herbaceous and woody plant communities in a Neotropical savanna.Crossref | GoogleScholarGoogle Scholar |