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Phenological and reproductive traits and their response to environmental variation differ among native and invasive grasses in a Neotropical savanna

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Abstract

Phenology is a key component of the life-history of plants, and non-native plant species with distinctive phenological traits may have an advantage over native species. In tropical savannas, water and light availability are often spatially and temporally heterogeneous, so that non-native species capable of changing their phenology in response to these factors are more likely to succeed in these ecosystems. We compared flowering onset and flowering period among African and native grasses in a Brazilian Neotropical savanna and assessed if these traits and the production of flowering tillers differ between two consecutive years and respond to spatial heterogeneity in water table depth and canopy closure. Non-native species showed multiple flowering patterns; Urochloa decumbens flowered from the mid-rainy season to the mid-dry season, Melinis minutiflora flowered during the dry season and Mepens repens flowered throughout the year. In addition, they were responsive to annual and abiotic variation, as U. decumbens also showed longer flowering period and produced more flowering tillers in the second year, except over shallow groundwater and high canopy closure, whereas M. minutiflora produced fewer flowering tillers under high canopy closure and M. repens showed large reproductive decline in the second year. Native grasses flowered in the middle of the rainy season regardless of annual and abiotic variation, although in the second year one species produced more flowering tillers in seasonally flooded sites. The phenology of M. repens is consistent with a ruderal life-history, so that it is only likely to become dominant under repeated disturbances. By contrast, the ability of changing flowering period and reproductive output according to growing conditions showed by U. decumbens and the distinct flowering timing showed by M. minutiflora may favour these species over less plastic native grasses, suggesting that phenological attributes contribute to the dominance of African grasses in Neotropical savannas.

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References

  • Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66

    Article  Google Scholar 

  • Alvares CA, Stape JL, Sentelhas PC et al (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728

    Article  Google Scholar 

  • Anderson JT, Inouye DW, McKinney AM, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc B Biol Sci 279:3843–3852

    Article  Google Scholar 

  • Archibald S, Scholes RJ (2007) Leaf green-up in a semi-arid African savanna -separating tree and grass responses to environmental cues. J Veg Sci 18:583–594

    Google Scholar 

  • Bates D, Maechler M, Bolker B, et al. (2016) Package ‘lme4’. R Package Version 1.1–10

  • Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64:261–273

    Article  Google Scholar 

  • Chambers LE, Altwegg R, Barbraud C et al (2013) Phenological changes in the southern hemisphere. PLoS ONE 8:e75514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman DS, Haynes T, Beal S et al (2014) Phenology predicts the native and invasive range limits of common ragweed. Glob Change Biol 20:192–202

    Article  Google Scholar 

  • Cianciaruso MV, Batalha MA, Silva IA (2005) Seasonal variation of a hyperseasonal cerrado in Emas National Park, central Brazil. Flora—Morphol Distrib Funct Ecol Plants 200:345–353

    Article  Google Scholar 

  • Cleland EE, Chuine I, Menzel A et al (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365

    Article  PubMed  Google Scholar 

  • Coutinho LM (1978) O conceito do cerrado. Rev Bras Bot 1:17–23

    Google Scholar 

  • Craine JM, Wolkovich EM, Gene Towne E et al (2012) Flowering phenology as a functional trait in a tallgrass prairie. New Phytol 193:673–682

    Article  PubMed  Google Scholar 

  • Dalgleish HJ, Ott JP, Setshogo MP et al (2012) Inter-specific variation in bud banks and flowering effort among semi-arid African savanna grasses. South Afr J Bot 83:127–133

    Article  Google Scholar 

  • Damasceno G, Souza L, Pivello VR et al (2018) Impact of invasive grasses on Cerrado under natural regeneration. Biol Invasions 20:3621–3629

    Article  Google Scholar 

  • D’Antonio CM, Hughes RF, Vitousek PM (2001) Factors influencing dynamics of two invasive C4 grasses in seasonally dry Hawaiian woodlands. Ecology 82:89–104

    Google Scholar 

  • David A, Menges E (2011) Microhabitat preference constrains invasive spread of non-native natal grass (Melinisrepens (Willd.) Zizka). Biol Invasions 13:2309–2322

    Article  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Dlugosch KM, Alice Cang F, Barker BS et al (2015) Evolution of invasiveness through increased resource use in a vacant niche. Nat Plants 1:15066

    Article  PubMed  PubMed Central  Google Scholar 

  • Elton CS (1958) The reasons for conservation. The ecology of invasions by animals and plants. Springer, Berlin, pp 143–153

    Book  Google Scholar 

  • Feng Y, Fouqueray TD, van Kleunen M (2019) Linking Darwin’s naturalisation hypothesis and Elton’s diversity–invasibility hypothesis in experimental grassland communities. J Ecol 107:794–805

    Article  Google Scholar 

  • França H, Ramos Neto MB, Setzer A (2007) O fogo no Parque Nacional das Emas. Ministério do Meio Ambiente, Brasília

    Google Scholar 

  • Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA), Version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University, Burnaby

    Google Scholar 

  • Godoy O, Castro-Diez P, Valladares F et al (2009a) Different flowering phenology of alien invasive species in Spain: evidence for the use of an empty temporal niche? Plant Biol 11:803–811

    Article  CAS  PubMed  Google Scholar 

  • Godoy O, Richardson DM, Valladares F et al (2009b) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103:485–494

    Article  PubMed  Google Scholar 

  • Goldstein LJ, Suding KN (2014) Intra-annual rainfall regime shifts competitive interactions between coastal sage scrub and invasive grasses. Ecology 95:425–435

    Article  PubMed  Google Scholar 

  • Goodland R, Ferri MG (1979) Ecologia do Cerrado. Editora da Universidade de São Paulo, São Paulo

    Google Scholar 

  • Gottsberger G, Silberbauer-Gottsberger I (2006) Life in the cerrado: a South American tropical seasonal vegetation. Origin, structure, dynamics and plant use. Reta Verlag, Ulm

    Google Scholar 

  • Grime JP (2001) Plant strategies, vegetation processes, and ecosystems properties. Wiley, Chichester

    Google Scholar 

  • Guan K, Wood EF, Medvigy D et al (2014) Terrestrial hydrological controls on land surface phenology of African savannas and woodlands. J Geophys Res Biogeosci 119:1652–1669

    Article  Google Scholar 

  • Higgins SI, Delgado-Cartay MD, February EC et al (2011) Is there a temporal niche separation in the leaf phenology of savanna trees and grasses? J Biogeogr 38:2165–2175

    Article  Google Scholar 

  • Hoffmann WA, Haridasan M (2008) The invasive grass, Melinis minutiflora, inhibits tree regeneration in a Neotropical savanna. Austral Ecol 33:29–36

    Article  Google Scholar 

  • Hoffmann WA, Lucatelli VMPC, Silva FJ et al (2004) Impact of the invasive alien grass Melinis minutiflora at the savanna-forest ecotone in the Brazilian Cerrado. Divers Distrib 10:99–103

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, et al. (2016) Package ‘multcomp’. Simultaneous inference in general parametric models. Project for statistical computing, Vienna

  • IFSP (2019) Dados meterologicos—Estação Ecologica de Itirapina. Instituto Florestal de São Paulo. http://www.iflorestal.sp.gov.br/Itirapina/dados_metereologicos.html. Accessed 15 Mar 2019

  • Klink CA, Joly CA (1989) Identification and distribution of C3 and C4 grasses in open and shaded habitats in Sao Paulo state, Brazil. Biotropica 21:30–34

    Article  Google Scholar 

  • Küster E, Durka W, Kühn I et al (2010) Differences in the trait compositions of non-indigenous and native plants across Germany. Biol Invasions 12:2001–2012

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Package ‘lmerTest’. R packageversion 2

  • Leite MB, Xavier RO, Oliveira PTS et al (2018) Groundwater depth as a constraint on the woody cover in a Neotropical Savanna. Plant and Soil 426:1–15

    Article  CAS  Google Scholar 

  • Lemos-Filho J, Barros C, Dantas G et al (2010) Spatial and temporal variability of canopy cover and understory light in a Cerrado of Southern Brazil. Braz J Biol 70:19–24

    Article  CAS  PubMed  Google Scholar 

  • Lustenhouwer N, Wilschut RA, Williams JL et al (2018) Rapid evolution of phenology during range expansion with recent climate change. Glob Change Biol 24:e534–e544

    Article  Google Scholar 

  • Munguía-Rosas MA, Ollerton J, Parra-Tabla V et al (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol Lett 14:511–521

    Article  PubMed  Google Scholar 

  • Munhoz CBR, Felfili JM (2005) Fenologia do estrato herbáceo-subarbustivo de uma comunidade de campo sujo na Fazenda Água Limpa no Distrito Federal, Brasil. Acta Bot Bras 19:979–988. https://doi.org/10.1590/S0102-33062005000400031

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Oliveira PTS, Leite MB, Mattos T et al (2017) Groundwater recharge decrease with increased vegetation density in the Brazilian cerrado. Ecohydrology 10:e1759. https://doi.org/10.1002/eco.1759

    Article  Google Scholar 

  • Parihar SS, Pathak PS (2006) Flowering phenology and seed biology of selected tropical perennial grasses. Tropic Ecol 47:1

    Google Scholar 

  • Pivello VG, Shida CN, Meirelles ST (1999) Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodivers Conserv 8:1281–1294

    Article  Google Scholar 

  • Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862

    Article  Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Ramos D, Diniz P, Valls JM (2014) Habitat filtering and interspecific competition influence phenological diversity in an assemblage of Neotropical savanna grasses. Braz J Bot 37:29–36

    Article  Google Scholar 

  • Sarmiento G (1983) Patterns of Specific and Phenological Diversity in the Grass Community of the Venezuelan Tropical Savannas. J Biogeogr 10:373–391

    Article  Google Scholar 

  • Sarmiento G (1984) The ecology of Neotropical Savannas. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Sarmiento G (1992) Adaptive strategies of perennial grasses in South American savannas. J Veg Sci 3:325–336

    Article  Google Scholar 

  • Seghieri J, Simier M (2002) Variations in phenology of a residual invasive shrub species in Sahelian fallow savannas, south-west Niger. J Trop Ecol 18:897–912

    Article  Google Scholar 

  • Silva DA (2005) Levantamento do meio físico das estações Ecológica e Experimental de Itirapina, São Paulo, Brasil. Rev Inst Florest 17:113–128

    Google Scholar 

  • Silva JF, Ataroff M (1985) Phenology, seed crop and germination of coexisting grass species from a tropical savanna in western Venezuela. Acta Oecol 6:41–51

    Google Scholar 

  • Stokes CA, MacDonald GE, Adams CR et al (2011) Seed biology and ecology of natalgrass (Melinis repens). Weed Sci 59:527–532

    Article  CAS  Google Scholar 

  • Vilà M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    Article  PubMed  Google Scholar 

  • Wadgymar SM, Ogilvie JE, Inouye DW et al (2018) Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment. New Phytol 218:517–529

    Article  PubMed  Google Scholar 

  • Wainwright CE, Wolkovich EM, Cleland EE (2012) Seasonal priority effects: implications for invasion and restoration in a semi-arid system. J Appl Ecol 49:234–241

    Article  Google Scholar 

  • Wickham H (2010) ggplot2: elegant graphics for data analysis. J Stat Softw 35:65–88

    Google Scholar 

  • Wickham H (2016) Francois R. dplyr: a grammar of data manipulation. R package version 0.5. 0. https://CRAN.R-project.org/package=dplyr

  • Williams D, Baruch Z (2000) African grass invasion in the Americas: ecosystem consequences and the role of ecophysiology. Biol Invasions 2:123–140

    Article  Google Scholar 

  • Wilsey BJ, Daneshgar PP, Polley HW (2011) Biodiversity, phenology and temporal niche differences between native- and novel exotic-dominated grasslands. Perspect Plant Ecol Evol Syst 13:265–276

    Article  Google Scholar 

  • Wolkovich EM, Cleland EE (2010) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294

    Article  Google Scholar 

  • Wolkovich EM, Cleland EE (2014) Phenological niches and the future of invaded ecosystems with climate change. AoB Plants. https://doi.org/10.1093/aobpla/plu013

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolkovich EM, Davies TJ, Schaefer H et al (2013) Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change. Am J Bot 100:1407–1421

    Article  PubMed  Google Scholar 

  • Xavier RO, Leite MB, Silva-Matos DM (2017) Stress responses of native and exotic grasses in a Neotropical savanna predict impacts of global change on invasion spread. Austral Ecol 42:562–576

    Article  Google Scholar 

  • Zenni RD, Sampaio AB, Lima YP et al (2019) Invasive Melinis minutiflora outperforms native species, but the magnitude of the effect is context-dependent. Biol Invasions 21:657–667

    Article  Google Scholar 

  • Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin

    Book  Google Scholar 

Download references

Acknowledgements

We are thankful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant 2011/21019-6) and the Coordenadoria de Aperfeiçoamento do Ensino Superior for the scholarship granted to the first and second author, respectively. DM. Silva Matos thanks the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico/CNPq (307839/2014-1). Managers of the Itirapina Ecological Station provided essential logistical and technical support, and L. A. Joaquim and Cidinei Messias de Souza (in memoriam) supported the fieldwork. We also thank C. Alba and an anonymous reviewer for their helpful comments and suggestions on the manuscript.

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  1. Department of Ecology, Biosciences Institute, University of São Paulo, Rua do matão 123, São Paulo, SP, 05508-090, Brazil

    Rafael de Oliveira Xavier

  2. Department of Hydrobiology, Federal University of São Carlos, Washington Luís Highway, km 235, São Carlos, SP, 13565-905, Brazil

    Rafael de Oliveira Xavier, Marcelo Boccia Leite & Dalva Maria da Silva Matos

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  1. Rafael de Oliveira Xavier
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Xavier, R.O., Leite, M.B. & da Silva Matos, D.M. Phenological and reproductive traits and their response to environmental variation differ among native and invasive grasses in a Neotropical savanna. Biol Invasions 21, 2761–2779 (2019). https://doi.org/10.1007/s10530-019-02013-w

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