Seasonal variation of a plant-pollinator network in the Brazilian Cerrado: Implications for community structure and robustness

Autoři: Simone Cappellari Rabeling aff001;  Jia Le Lim aff002;  Rosana Tidon aff003;  John L. Neff aff004;  Beryl B. Simpson aff001;  Samraat Pawar aff005
Působiště autorů: Department of Integrative Biology, The University of Texas at Austin, Texas, United States of America aff001;  Department of Life Sciences, South Kensington Campus, Imperial College London, London, United Kingdom aff002;  Departamento de Genética e Morfologia, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, DF, Brazil aff003;  Central Texas Melittological Institute, Austin, TX, United States of America aff004;  Department of Life Sciences, Silwood Park Campus, Imperial College London, Ascot, Berkshire, United Kingdom aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224997


Seasonal variation in the availability of floral hosts or pollinators is a key factor influencing diversity in plant-pollinator communities. In seasonally dry Neotropical habitats, where month-long periods of extreme drought are followed by a long rainy season, flowering is often synchronized with the beginning of precipitation, when environmental conditions are most beneficial for plant reproduction. In the Brazilian Cerrado, a seasonally dry ecosystem considered one of the world’s biodiversity hotspots for angiosperms, plants with shallow root systems flower predominantly during the rainy season. Foraging activity in social bees however, the major pollinators in this biome, is not restricted to any particular season because a constant supply of resources is necessary to sustain their perennial colonies. Despite the Cerrado’s importance as a center of plant diversity, the influence of its extreme cycles of drought and precipitation on the dynamics and stability of plant-pollinator communities is not well understood. We sampled plant-pollinator interactions of a Cerrado community weekly for one year and used network analyses to characterize intra-annual seasonal variation in community structure. We also compared seasonal differences in community robustness to species loss by simulating extinctions of plants and pollinators. We find that the community shrinks significantly in size during the dry season, becoming more vulnerable to disturbance due to the smaller pool of floral hosts available to pollinators during this period. Major changes in plant species composition but not in pollinators has led to high levels of turnover in plant-pollinator associations across seasons, indicated by in interaction dissimilarity (<3% of shared interactions). Aseasonal pollinators, which mainly include social bees and some solitary specialized bees, functioned as keystone species, maintaining robustness during periods of drastic changes in climatic conditions.

Klíčová slova:

Bees – Community ecology – Community structure – Flowering plants – Plants – Seasonal variations – Seasons – Species interactions


1. Fryxell JM, Sinclair ARE. Causes and consequences of migration by large herbivores. Trends Ecol Evol. 1988;3: 237–41. doi: 10.1016/0169-5347(88)90166-8 21227239

2. Bell RH. A grazing ecosystem in the Serengeti. Sci Am. 1971;225: 86–93.

3. Gottsberger G. Some pollination strategies in neotropical savannas and forests. Plant Syst Evol. 1986;152: 29–45.

4. Bullock SH, Mooney HA, Medina E. Seasonally dry tropical forests: Cambridge University Press; 1995.

5. Morellato LPC, Alberton B, Alvarado ST, Borges B, Buisson E, Camargo MGG, et al. Linking plant phenology to conservation biology. Biol Conserv. 2016;195: 60–72.

6. Pennington RT, Lewis GP, Ratter JA. An overview of the plant diversity, biogeography and conservation of neotropical savannas and seasonally dry forests. In: Pennington RT, Lewis GP, Ratter JA, editors. Neotropical savannas and seasonally dry forests. Boca Raton: CRC press; 2006. pp. 17–45.

7. Huber O. Neotropical savannas: their flora and vegetation. Trends Ecol Evol. 1987;2: 67–71. doi: 10.1016/0169-5347(87)90151-0 21227819

8. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403: 853. doi: 10.1038/35002501 10706275

9. Vilela AA, Del Claro VTS, Torezan-Silingardi HM, Del-Claro K. Climate changes affecting biotic interactions, phenology, and reproductive success in a savanna community over a 10-year period. Arthropod Plant Interact. 2018;12: 215–27.

10. Ricklefs RE, Renner SS. Species richness within families of flowering plants. Evol. 1994;48: 1619–36.

11. Antonelli A, Sanmartín I. Why are there so many plant species in the Neotropics? Taxon. 2011;60: 403–14.

12. Bawa KS. Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst. 1990;21: 399–422.

13. Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120: 321–6.

14. Kay KM, Sargent RD. The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annu Rev Ecol Evol Syst. 2009;40: 637–56.

15. Ratter JA, Bridgewater S, Ribeiro JF. Biodiversity patterns of the woody vegetation of the Brazilian Cerrado. In: Pennington RT, Lewis GP, Ratter JA, editors. Neotropical savannas and seasonally dry forests. Boca Raton: CRC press; 2006. pp. 31–65.

16. Gottsberger G, Silberbauer-Gottsberger I. Life in the Cerrado: origin, structure, dynamics and plant use. Vol 1. Ulm: Reta Verlag; 2006.

17. Silveira F, Campos MdO. A melissofauna de Corumbataí (SP) e Paraopeba (MG) e uma análise da biogeografia das abelhas do cerrado brasileiro (Hymenoptera, Apoidea). Rev Bras Entomol. 1995;39: 371–401.

18. Pinheiro-Machado C, Alves-dos-Santos I, Imperatriz-Fonseca VL, Kleinert AdMP, Silveira F. Brazilian bee surveys: state of knowledge, conservation and sustainable use. In: Kevan PG, Imperatriz-Fonseca VL, editors. Pollinating bees: the conservation link between agriculture and nature. Brasília: Ministério do Meio Ambiente; 2002. pp.115–29.

19. Silveira FA, Melo GA, Almeida EA. Abelhas brasileiras: sistemática e identificação. Belo Horizonte: Fundação Araucária; 2002.

20. Oliveira PE, Gibbs PE. Reproductive biology of woody plants in a cerrado community of Central Brazil. Flora. 2000;195: 311–29.

21. Oliveira PE, Gibbs PE. Pollination and reproductive biology in cerrado plant communities. In: Oliveira PS, Marquis RJ, editors. The cerrados of Brazil: ecology and natural history of a neotropical savanna. New York: Columbia University Press; 2002. pp. 329–47.

22. Silberbauer-Gottsberger I, Gottsberger G. A polinização de plantas do cerrado. Rev Bras Biol. 1988;48: 651–63.

23. Gottsberger G, Silberbauer-Gottsberger I. Life in the Cerrado: pollination and seed dispersal. Vol 2. Ulm: Reta Verlag; 2006.

24. Martins F, Batalha M. Pollination systems and floral traits in cerrado woody species of the Upper Taquari region (Central Brazil). Braz J Biol. 2006;66: 543–52. doi: 10.1590/s1519-69842006000300021 16862310

25. Pinheiro F, Diniz I, Coelho D, Bandeira M. Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecol. 2002;27: 132–36.

26. Tidon R. Relationships between drosophilids (Diptera, Drosophilidae) and the environment in two contrasting tropical vegetations. Biol J Linn Soc Lond. 2006;87: 233–47.

27. Valadão H, Hay JDV, Tidon R. Temporal dynamics and resource availability for drosophilid fruit flies (Insecta, Diptera) in a gallery forest in the Brazilian Savanna. International Journal of Ecology. 2010;2010.

28. Roque F, Mata RAd, Tidon R. Temporal and vertical drosophilid (Insecta; Diptera) assemblage fluctuations in a neotropical gallery forest. Biodivers Conserv. 2013;22: 657–72.

29. Mata RAd, Valadão H, Tidon R. Spatial and temporal dynamics of drosophilid larval assemblages associated to fruits. Rev Bras Entomol. 2015;59: 50–7.

30. Eiten G. The cerrado vegetation of Brazil. Bot Rev. 1972;38: 201–341.

31. Batalha MA, Martins FR. Reproductive phenology of the cerrado plant community in Emas National Park (central Brazil). Aust J Bot. 2004;52: 149–61.

32. Mantovani W, Martins FR. Variações fenológicas das espécies do cerrado da Reserva Biológica de Moji Guaçu. Rev Bras Bot. 1988;11: 101–12.

33. Meinzer FC, Andrade JL, Goldstein G, Holbrook NM, Cavelier J, Wright SJ. Partitioning of soil water among canopy trees in a seasonally dry tropical forest. Oecologia. 1999;121: 293–301. doi: 10.1007/s004420050931 28308316

34. Jackson PC, Meinzer FC, Bustamante M, Goldstein G, Franco A, Rundel PW, et al. Partitioning of soil water among tree species in a Brazilian Cerrado ecosystem. Tree Physiol. 1999;19: 717–24. doi: 10.1093/treephys/19.11.717 12651310

35. Rawitscher F. The water economy of the vegetation of the Campos Cerrados' in Southern Brazil. J Ecol. 1948: 237–68.

36. Ferri MG. Transpiração de plantas permanentes dos "Cerrados". PhD Thesis, Universidade de São Paulo. Boletim da Faculdade de Filosofia, Ciências e Letras, Botânica. 1944: 155–224.

37. Oliveira P. Fenologia e biologia reprodutiva de espécies do Cerrado. In: Sano SM, editor. Cerrado: ecologia e flora. Brasília: Embrapa; 2008. pp. 273–90.

38. Cappellari SC. Polinização na área de proteção ambiental Gama-Cabeça-de-Viado e sua importância para a conservação do Cerrado. In: Brito MCL, editor. Reserva Ecológica do IBGE: Diversidade Terrestre, Vol. 1. Rio de Janeiro: Brazilian Institute of Geography and Statistics (IBGE); 2011. pp. 275–297.

39. Burkle LA, Alarcón R. The future of plant–pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot. 2011;98: 528–38. doi: 10.3732/ajb.1000391 21613144

40. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. Generalization in pollination systems, and why it matters. Ecology. 1996;77: 1043–60.

41. CaraDonna PJ, Petry WK, Brennan RM, Cunningham JL, Bronstein JL, Waser NM, et al. Interaction rewiring and the rapid turnover of plant–pollinator networks. Ecol Lett. 2017;20: 385–94. doi: 10.1111/ele.12740 28156041

42. Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD. Long‐term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett. 2008;11: 564–75. doi: 10.1111/j.1461-0248.2008.01170.x 18363716

43. Waser NM. Specialization and generalization in plant-pollinator interactions: a historical perspective. In: Waser NM, Ollerton J, editors. Plant-pollinator interactions: from specialization to generalization. Chicago: University of Chicago Press; 2006. pp. 3–17.

44. Oliveira-Filho AT, Ratter JA. Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira PS, Marquis RJ, editors. The cerrados of Brazil: ecology and natural history of a neotropical savanna. New York: Columbia University Press; 2002. pp. 91–120.

45. Moure JS. As mamangabas sociais do Brasil (Bombus Latr.) (Hym., Apoidea). Rio de Janeiro: Editora Vozes Ltda.; 1962.

46. Aguiar AJ, Melo GA. Revision and phylogeny of the bee genus Paratetrapedia Moure, with description of a new genus from the Andean Cordillera (Hymenoptera, Apidae, Tapinotaspidini). Zool J Linn Soc. 2011;162: 351–442.

47. Moure JS, Urban D, Melo G. Catalogue of bees (Hymenoptera, Apoidea) in the Neotropical region. Curitiba: Sociedade Brasileira de Entomologia; 2007.

48. Michener C. The Bees of the World. 2nd edition. Baltimore: John Hopkins Press. 2007.

49. Thébault E, Fontaine C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science. 2010;329: 853–6. doi: 10.1126/science.1188321 20705861

50. Vázquez DP, Morris WF, Jordano P. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett. 2005;8: 1088–94.

51. Almeida‐Neto M, Guimaraes P, Guimaraes PR Jr, Loyola RD, Ulrich W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos. 2008;117: 1227–39.

52. Bascompte J, Jordano P, Melián CJ, Olesen JM. The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA. 2003;100: 9383–9387. doi: 10.1073/pnas.1633576100 12881488

53. Rohr RP, Saavedra S, Bascompte J. On the structural stability of mutualistic systems. Science. 2014;345: 1253497. doi: 10.1126/science.1253497 25061214

54. Pawar S. Why are plant-pollinator networks nested? Science. 2014;345: 383. doi: 10.1126/science.1256466 25061191

55. Whittaker RH. Vegetation of the Siskiyou mountains, Oregon and California. Ecol Monogr. 1960;30: 279–338.

56. Poisot T, Canard E, Mouillot D, Mouquet N, Gravel D. The dissimilarity of species interaction networks. Ecol Lett. 2012;15:1353–61. doi: 10.1111/ele.12002 22994257

57. Koleff P, Gaston KJ, Lennon JJ. Measuring beta diversity for presence–absence data. J Anim Ecol. 2003;72: 367–82.

58. Dehmer M, Emmert-Streib F, Graber A, Salvador A. Applied statistics for network biology: methods in systems biology: John Wiley & Sons; 2011.

59. Dunne JA, Williams RJ, Martinez ND. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett. 2002;5: 558–67.

60. Memmott J, Waser NM, Price MV. Tolerance of pollination networks to species extinctions. Proc Biol. 2004;271: 2605–11.

61. Memmott J, Craze PG, Waser NM, Price MV. Global warming and the disruption of plant–pollinator interactions. Ecol Lett. 2007;10: 710–17. doi: 10.1111/j.1461-0248.2007.01061.x 17594426

62. Kaiser‐Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett. 2010;13: 442–52. doi: 10.1111/j.1461-0248.2009.01437.x 20100244

63. Medan D, Basilio AM, Devoto M, Bartoloni NJ, Torretta JP, Petanidou T. Measuring generalization and connectance in temperate, year-long active systems. In: Waser NM, Ollerton J, editors. Plant-pollinator interactions: from specialization to generalization. Chicago: University of Chicago Press; 2006. pp. 245–59.

64. Roubik DW. Ecology and natural history of tropical bees: Cambridge University Press; 1992.

65. Biesmeijer JC, Slaa EJ. The structure of eusocial bee assemblages in Brazil. Apidologie. 2006;37: 240–58.

66. Neff JL, Simpson BB. Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematics. J Kans Entomol Soc. 1981;54: 95–123.

67. Simpson BB, Neff JL. Floral rewards: alternatives to pollen and nectar. Ann Mo Bot Gard. 1981; 68:301–22.

68. Vogel S. Ölblumen und ölsammelnde Bienen. Tropische und subtropische Pflanzenwelt. Wiesbaden: Akademie der Wissenschaften und der Literatur Mainz Franz Steiner Verlag; 1974.

69. Alarcón R, Waser NM, Ollerton J. Year‐to‐year variation in the topology of a plant–pollinator interaction network. Oikos. 2008;117: 1796–807.

70. Souza CS, Maruyama PK, Aoki C, Sigrist MR, Raizer J, Gross CL, et al. Temporal variation in plant–pollinator networks from seasonal tropical environments: higher specialization when resources are scarce. J Ecol. 2018;106: 2409–2420.

71. Basilio AM, Medan D, Torretta JP, Bartoloni NJ. A year‐long plant‐pollinator network. Austral Ecol. 2006;31: 975–83.

72. Lundgren R, Olesen JM. The dense and highly connected world of Greenland’s plants and their pollinators. Arct Antarct Alp Res. 2005;37: 514–20.

73. Olesen JM, Bascompte J, Elberling H, Jordano P. Temporal dynamics in a pollination network. Ecology. 2008;89: 1573–82. doi: 10.1890/07-0451.1 18589522

74. Jordano P, Bascompte J, Olesen JM. Invariant properties in coevolutionary networks of plant–animal interactions. Ecol Lett. 2003;6: 69–81.

75. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP. Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot. 2009;103: 1445–57. doi: 10.1093/aob/mcp057 19304996

76. Coutinho LM. O conceito do cerrado. Rev Bras Bot. 1978;1: 17–23.

77. Armbruster WS. Evolutionary and ecological aspects of specialized pollination: views from the arctic to the tropics. In: Waser NM, Ollerton J, editors. Plant-pollinator interactions: from specialization to generalization. Chicago: University of Chicago Press; 2006. pp. 260–82.

78. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc Natl Acad Sci USA. 2008;105: 17029–33. doi: 10.1073/pnas.0806446105 18955707

79. Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421: 37. doi: 10.1038/nature01286 12511946

80. Chambers LE, Altwegg R, Barbraud C, Barnard P, Beaumont LJ, Crawford RJ, et al. Phenological changes in the southern hemisphere. PLoS One. 2013;8: e75514. doi: 10.1371/journal.pone.0075514 24098389

81. Velazco SJE, Villalobos F, Galvão F, De Marco Júnior P. A dark scenario for Cerrado plant species: Effects of future climate, land use and protected areas ineffectiveness. Divers Distrib. 2019;25: 660–73.

Článek vyšel v časopise


2019 Číslo 12