Phenology Patterns Across a Rupestrian Grassland Altitudinal Gradient



Phenology is the study of recurrent biological events in the life cycle of organisms. For plants, reproductive events such as flowering and fruiting are critical stages in their life cycles, which also greatly affect other organisms depending on these resources. Here, we present the first community level plant phenology study across an altitudinal gradient from cerrado through rupestrian grassland to higher altitudinal grasslands developed in the South Espinhaço Mountain range (Serra do Cipó, Brazil). We describe the seasonal patterns of flowering and fruiting phenology and discuss the dependency of reproductive events on the varying climate and habitat types across the gradient. We point out the importance of long-term monitoring and further detailed analyses of families and species contribution to unravel the structure of community phenology, the environmental drivers and sensitivity to climate changes.


Reproductive phenology Seasonality patters Altitudinal grasslands Cerrado 



We thank the many stakeholders that have allowed us to work in their lands and for logistical support: Serra Morena Inn, Cedro Cachoeira Textile Industry, Vellozia Reserve, Pedra do Elefante Inn, Eduardo C. Costa Jr, and Serra do Cipó National Park. We are grateful to Ana Cláudia Rodrigues, Valeria Campos, Natalia Costa Soares, Bruna Alberton, Irene Mendoza, Eduardo A. Athayde, Júlia Santos, Swanni Alvarado, Eli Garcia, Márcio Schafer Annia Susin, Thiago Horta, Leonardo F. Cancian, and Fernando Silveira for assistance in the field and to Ramiro Aguilar for valuable comments on the text. This research was supported by São Paulo Research Foundation FAPESP (FAPESP-VALE-FAPEMIG grant #2010/51307-0 and grant #2009/54208-6); Rocha, N.M.W.B. and Carstensen, D.W. received fellowships from FAPESP grants #2011/22635-2 and #2012/12429-9. Fernandes, GW thanks the grants and logistic supported provided by CNPq, Fapemig and Reserva Vellozia. Morellato, L.P.C. and Fernandes, GW received CNPq research productivity fellowship.


  1. Aizen MA (2003) Influences of animal pollination and seed dispersal on winter flowering in a temperate Misteltoe. Ecology 84:2613–2627CrossRefGoogle Scholar
  2. Alvarado ST, Buisson E, Rabarison H, Rajeriarison C, Birkinshaw C, Lowry PP, Morellato LP (2014) Fire and the reproductive phonology of endangered Madagascar sclerophyllous tapia woodlands. South Afr J Bot 94:79–87Google Scholar
  3. Barrère M (1992) Terra, patrimônio comum: a ciência a serviço do meio ambiente e do desenvolvimento. Nobel, São PauloGoogle Scholar
  4. Batalha MA, Mantovani W (2000) Reproductive phenological patterns of cerrado plant species at the Pe-de-Gigante reserve (Santa Rita do Passa Quatro, SP, Brazil): A comparison between the herbaceous and woody floras. Rev Bras Biol 60:129–145CrossRefPubMedGoogle Scholar
  5. Batalha MA, Aragaki S, Mantovani W (1997) Variações fenológicas das espécies do cerrado em Emas (Pirassununga, SP). Acta Bot Bras 11:61–78Google Scholar
  6. Belo RM, Negreiros D, Fernandes GW, Silveira FAO, Ranieri BD, Morellato LPC (2013) Fenologia reprodutiva e vegetativa de arbustos endêmicos de campo rupestre na Serra do Cipó, Sudeste do Brasil. Rodriguésia 64:817–828CrossRefGoogle Scholar
  7. Bhattarai KR, Vetaas OL (2003) Variation in plant species richness of different life forms along a subtropical elevation gradient in the Himalayas, east Nepal. Glb Ecol Biogeogr 12:327–340CrossRefGoogle Scholar
  8. Borges DFdM (2011) Padrões de variação na riqueza de espécies em gradientes altitudinais: uma revisão multi-taxonômica. MSc Dissertation, Universidade de Brasília, BrasíliaGoogle Scholar
  9. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortiek CJ, Michalet R, Paolini L, Pugnaireq FI, Newingham B, Aschehoug ET, Armasq C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefPubMedGoogle Scholar
  10. Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont LJ, Crawford RJM, Durant JM, Hughes L, Keatley MR, Low M, Morellato PC, Poloczanska ES, Ruoppolo V, Vanstreels RET, Woehler EJ, Wolfaardt AC (2013) Phenological changes in the southern hemisphere. Plos One 8:e75514. doi: 10.71371/journal.pone.0075514
  11. Conceição AA, Funch LS, Pirani JR (2007) Reproductive phenology, pollination and seed dispersal syndromes on sandstone outcrop vegetation in the “Chapada Diamantina”, northeastern Brazil: population and community analyses. Rev Bras Bot 30:475–485Google Scholar
  12. Dutra VF, Vieira MF, Garcia FCP, Lima HCL (2009) Fenologia reprodutiva, sindromes de polinização e dispersão em espécies de Leguminosae dos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguesia 60:371–387Google Scholar
  13. Fernandes GW, Barbosa NP, Negreiros D, Paglia AP (2014) Challenges for the conservation of vanishing megadiverse rupestrian grasslands. Natureza Conservação 12(2):162–165 Google Scholar
  14. Fiaschi P, Jr Pirani (2005) Flora da Serra do Cipó, Minas Gerais: Araliaceae. Bol Bot Univ São Paulo 23:267–275Google Scholar
  15. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in lowlands of Costa Rica. J Ecol 62:881–919CrossRefGoogle Scholar
  16. Giulietti AM, Jr Pirani (1988) Patterns of geographical distribution of some plant species from Espinhaço range, Minas Gerais and Bahia, Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a workshop on Neotropical distribution patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp 39–69Google Scholar
  17. Giulietti AM, Menezes NL, Pirani JR, Meguro M, Wanderley MGL (1987) Flora da Serra do Cipó, Minas Gerais: caracterização e lista de espécies. Bol Bot Univ São Paulo 9:1–151Google Scholar
  18. Groppo M, Jr Pirani (2005) Flora da Serra do Cipó, Minas Gerais: Aquifoliaceae. Bol Bot Univ São Paulo 23:257–265Google Scholar
  19. Groppo M, Amaral MM, Ceccantini GCT (2007) Flora da Serra do Cipó, Minas Gerais: Apodanthaceae (Rafflesiaceae s.l.), e notas sobre a anatomia de Pilostyles. Bol. Bol Bot Univ São Paulo 25:81–86Google Scholar
  20. Humboldt AV, Bonpland A (1807) Essai sur la géographie des plantes. ccompagné d’um tableau physique des régions equinoxiales. Editorial Cultura, Mexico CityGoogle Scholar
  21. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefPubMedGoogle Scholar
  22. Kinoshita LS, Simões AO (2005) Flora da Serra do Cipó, Minas Gerais: Apocynoideae s.str. (Rauvolfioideae e Apocynoideae). Bol Bot Univ São Paulo 23:235–256Google Scholar
  23. Köppen W (1948) Climatologia. Fundo de Cultura Economica, MexicoGoogle Scholar
  24. Le Stradic S (2012) Composition, phenology and restoration of campo rupestre mountain grasslands—Brazil. PhD thesis, Universidade Federal de Minas Gerais and Université d’Avignon et des Pays de Vaucluse, Belo HorizonteGoogle Scholar
  25. Le Stradic S, Buisson E, Fernandes GW (2015) Vegetation composition and structure of some Neoptropical grasslands in Brazil. J Mt Sci 12:864–877CrossRefGoogle Scholar
  26. Lieberman D, Lieberman M, Peralta R, Hartshorn GS (1996) Tropical forest structure and composition on a large-scale altitudinal gradient in Costa Rica. J Ecol 84:137–152CrossRefGoogle Scholar
  27. Lobo JA, Quesada M, Stoner KE, Fuchs EJ, Herreiras-Diego Y, Rojas J, Saborio G (2003) Factor affecting phenological patterns of bombacaceous trees in seasonal forests in Costa Rica and Mexico. Am J Bot 90:1054–1063CrossRefPubMedGoogle Scholar
  28. Madeira JA, Fernandes GW (1999) Reproductive phenology of sympatric taxa of Chamaecrista (Leguminosae) in Serra do Cipo, Brazil. J Trop Ecol 15:463–479CrossRefGoogle Scholar
  29. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kuebler K, Bissolli P, Og Braslavska, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F-E, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glb Chan Biol 12:1969–1976CrossRefGoogle Scholar
  30. Morellato LPC (1995) As estações do ano na floresta. In: Morellato PC, Leitão-Filho HF (eds) Ecologia e preservação de uma floresta tropical urbana. Editora Unicamp, Campinas, pp 37–41Google Scholar
  31. Morellato LPC, Leitão-Filho HF (1992) Padrões de frutificação e dispersão na Serra do Japi. In: Morellato LPC (ed) História natural da Serra do Japi: ecologia e preservação de uma área florestal no sudeste do Brasil. Editora da Unicamp - FAPESP, Campinas, pp 112–140Google Scholar
  32. Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823CrossRefGoogle Scholar
  33. Morellato LPC, Gressler E, Camargo MGG (2013) A review of plant phenology in South and Central America. In: Schwartz MD (ed) Phenology: an integrative environmental science, 2nd edn. Springer, The Neederlands, pp 91–113CrossRefGoogle Scholar
  34. Morellato LPC, Alberton B, Alvarado ST, Borges BD, Buisson E, Camargo MGG, Cancian LF, Carstensen DW, Escobar D FE, Leite PTP, Mendoza I, Rocha NMWB, Silva TSF, Soares NC, Staggemeier VG, Streher AS, Vargas BC, Peres CA (2016) Linking plant phenology to conservation biology. Biol Cons 195:60–72Google Scholar
  35. Morisette JT, Richardson AD, Knapp AK, Fisher JI, Graham EA, Abatzoglou J, Wilson BE, Breshears DD, Henebry GM, Hanes JM, Liang L (2009) Tracking the rhythm of the seasons in the face of global change: phenological research in the 21st century. Front Ecol Environ 7:253–260CrossRefGoogle Scholar
  36. Neves SPS (2009) Fenologia, biologia floral e polinização de espécies de Velloziaceae Endl. em área de campo rupestre na Chapada Diamantina, Bahia, Brasil. MSc Dissertation, Universidade Estadual de Feria de Santana, Feira de SantanaGoogle Scholar
  37. Nunes YRF, Landau EC, Veloso MDM (2008) Diversidade de Melastomataceae em diferentes altitudes de campos rupestres na Serra do Cipó, MG. Unim Cien 10:34–45Google Scholar
  38. Oliveira PEAM, Moreira AG (1992) Anemocoria em espécies de cerrado e mata de galeria de Brasília, DF. Rev Bras Bot 15:163–174Google Scholar
  39. Pereira AR, Angelocci LR, Sentelhas PC (2002) Agrometeorologia: fundamentos e aplicações práticas agropecuária. Editora Agopecuária, Guaíba, RS, 478 ppGoogle Scholar
  40. Rosenzweig C, Karoly D, Vicarelli M, Neofotis P, Wu Q, Casassa G, Menzel A, Root TL, Estrella N, Seguin B, Tryjanowski P, Liu C, Rawlins S, Imeson A (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353–357CrossRefPubMedGoogle Scholar
  41. Schwartz MD (2013) Phenology: an integrative environmental science, 2nd edn. Springer, The NeederlandsCrossRefGoogle Scholar
  42. Silveira FAO, Ribeiro RC, Oliveira DMT, Fernandes GW, Lemos-Filho JP (2011) Evolution of physiological dormancy multiple times in Melastomataceae from Neotropical montane vegetation. Seed Sci Res 22:37–44CrossRefGoogle Scholar
  43. Silveira FO, Santos J, Franceschinelli EV, Morellato LPC, Fernandes GW (2015) Costs and benefits of reproducing under unfavorable conditions: an integrated view of ecological and physiological constraints in a cerrado shrub. Plant Ecol 216:963–974CrossRefGoogle Scholar
  44. Silveira F, Negreiros D, Barbosa N, Buisson E, Carmo F, Carstensen D, Conceição A, Cornelissen T, Echternacht L, Fernandes GW, Garcia Q, Guerra T, Jacobi C, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves F, Oliveira R, Schaefer C, Viana P, Lambers H (2016) Ecology and evolution of the endangered campo rupestre: a neglected biodiversity conservation priority. Plant Soil. doi: 10.1007/s11104-015-2637-8 Google Scholar
  45. Staggemeier VG, Diniz JAF, Morellato LPC (2010) The shared influence of phylogeny and ecology on the reproductive patterns of Myrteae (Myrtaceae). J Ecol 98:1409–1421CrossRefGoogle Scholar
  46. Staggemeier VG, Diniz-Filho JAF, Zipparro VB, Gressler E, de Castro ER, Mazine F, da Costa IR, Lucas E, Morellato LPC (2015) Clade-specific responses regulate phenological patterns in Neotropical Myrtaceae. Persp Plant Ecol Evol Syst 17:476–490Google Scholar
  47. Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S, Fernandes GW, Durigan G, Buisson E, Putz FE, Bond WJ (2015a) Tyranny of trees in grassy biomes. Science 347:484–485CrossRefPubMedGoogle Scholar
  48. Veldman JW, Buisson E, Durigan G, Fernandes GW, Le Stradic S, Mahy G, Negreiros D, Overbeck GE, Veldman RG, Zaloumis NP, Putz FE, Bond WJ (2015b) Toward an old-growth concept for grasslands, savannas, and woodlands. Front Ecol Environ 13:154–162CrossRefGoogle Scholar
  49. Venn S, Pickering C, Green K (2012) Short-term variation in species richness across an altitudinal gradient of alpine summits. Biodiv Cons 21:3157–3186CrossRefGoogle Scholar
  50. Wolkovich EM, Cook BI, Davies TJ (2014) Progress towards an interdisciplinary science of plant phenology: building predictions across space, time and species diversity. New Phytol 201:1156–1162CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Departamento de BotânicaUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  2. 2.Ecologia Evolutiva & Biodiversidade/DBG, CP 486, ICBUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  3. 3.Department of BiologyStanford UniversityStanfordUSA
  4. 4.Gembloux Agro-Bio Tech Université de Liège, Biodiversité et PaysageGemblouxBelgium
  5. 5.Université D’Avignon et Des Pays Du Vaucluse, IMBE, CNRS, IRD, Aix Marseille Université, IUT D’AvignonAvignon Cedex 9France

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