Plant Ecology

, Volume 188, Issue 2, pp 265–275

Phenological patterns of Ficus citrifolia (Moraceae) in a seasonal humid-subtropical region in Southern Brazil

  • Rodrigo Augusto Santinelo Pereira
  • Efraim Rodrigues
  • Ayres de Oliveira MenezesJr
Original Paper

Abstract

Year-round flowering is widely reported in fig trees and is necessary for the survival of their short-living, specialized Agaonid pollinators. However, seasonality in both fig and leaf production has been noted in almost all published phenological studies. We have addressed the following questions in the present study: (1) Are reproductive and vegetative phenologies seasonal and, consequently, related to climate? (2) Does Ficus citrifolia produce ripe figs year round? (3) Is the fig development related to climate? And, (4) Are reproductive and vegetative phenologies independent? By investigating these questions with a F. citrifolia population over a two-year period, at the southern edge of the tropical region in Brazil, we detected phenological seasonality that was significantly correlated with climate. Our findings can be summarized as follows: (1) Trees became deciduous during the cold and dry months; (2) The flowering onset was asynchronous among individuals, but with moderate concentration during the hot and rainy months; (3) There was a correlation between the onset of flowering and vegetative phenology, with significantly higher crop initiations in individuals with full-leaf canopy; (4) Fig developmental time was longer in cold months; and (5) Ripe fig production occurred year-round and was not correlated with climate. Our results suggest that there are strong selection pressures that maintain the year-round flowering phenology in figs, for we have observed little seasonality in the phenology of such species despite the strong seasonality in the environment.

Keywords

Climate Fig phenology Generalized least squares Keystone species Mutualism Temporal auto-correlation 

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References

  1. Anstett MC, Hossaert-McKey M, Kjellberg F (1997). Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends Ecol Evol 12:94–99CrossRefGoogle Scholar
  2. Borchert R (1983). Phenology and control of flowering in tropical trees. Biotropica 15:81–89CrossRefGoogle Scholar
  3. Bronstein JL (1989) A mutualism at the edge of its range. Experientia 45:622–639CrossRefGoogle Scholar
  4. Bronstein JL, Gouyon PH, Gliddon C, Kjellberg F, Michaloud G (1990) The ecological consequences of flowering asynchrony in monoecious figs: a simulation study. Ecology 71:2145–2156CrossRefGoogle Scholar
  5. Corlett RT (1984) The phenology of Ficus benjamina and Ficus microcarpa in Singapore. J Singapore Natl Acad Sci 13:30–31Google Scholar
  6. Corlett RT (1987) The phenology of Ficus fistulosa in Singapore. Biotropica 19:122–124CrossRefGoogle Scholar
  7. Corlett RT (1993) Sexual dimorphism in the reproductive phenology of Ficus grossularioides Burm. f. in Singapore. Malayan Nat J 46:149–155Google Scholar
  8. Corrêa AR, Godoy H, Bernardes LRM (1982) Características climáticas de Londrina. IAPAR, CuritibaGoogle Scholar
  9. Crawley MJ (1993) GLIM for ecologists. Blackwell Scientific, OxfordGoogle Scholar
  10. Damstra KSJ, Richardson S, Reeler B (1996) Synchronized fruiting between trees of Ficus thonningii in seasonally dry habitats. J Biogeogr 23:495–500CrossRefGoogle Scholar
  11. DeWolf GP (1960) Ficus (Tourn.) L. Ann Miss Bot Garden 47:146–165Google Scholar
  12. Figueiredo RA, Sazima M (1997) Phenology and pollination ecology of three Brazilian fig species (Moraceae). Bot Acta 110:73–78Google Scholar
  13. Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–913CrossRefGoogle Scholar
  14. Galil J, Eisikowitch D (1968a) Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytol 67:745–758CrossRefGoogle Scholar
  15. Galil J, Eisikowitch D (1968b) On the pollination ecology of Ficus sycomorus in east Africa. Ecology 49:259–269CrossRefGoogle Scholar
  16. Galil J, Zeroni M, Bar-Shalom D (1973) Carbon dioxide and ethylene effects in the coordination between the pollinator Blastophaga quadraticeps and the syconium in Ficus religiosa. New Phytol 72:1113–1127CrossRefGoogle Scholar
  17. Galindo-Gonzalez J, Guevara S, Sosa VJ (2000) Bat- and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conserv Biol 14:1693–1703CrossRefGoogle Scholar
  18. Guevara S, Laborde J, Sánchez-Rios G (2004) Rain forest regeneration beneath the canopy of fig trees isolated in pastures of Los Tuxtlas, Mexico. Biotropica 36:99–108CrossRefGoogle Scholar
  19. Harrison RD (2001) Drought and the consequences of El Niño in Borneo: a case study of figs. Popul Ecol 43:63–75CrossRefGoogle Scholar
  20. Harrison RD, Yamamura N, Inoue T (2000) Phenology of a common roadside fig in Sarawak. Ecol Res 15:47–61CrossRefGoogle Scholar
  21. Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51CrossRefGoogle Scholar
  22. Kannan R, James DA (1999) Fruiting phenology and the conservation of the Great Pied Hornbill (Buceros bicornis) in the Western Ghats of southern India. Biotropica 31:167–177Google Scholar
  23. Kinnaird MF, Oȁ9Brien TG, Suryadi S (1996) Population fluctuation in Sulawesi Red-Knobbed Hornbills: tracking figs in space and time. The Auk 113:431–440Google Scholar
  24. Kjellberg F, Maurice S (1989) Seasonality in the reproductive phenology of Ficus: its evolution and consequences. Experientia 45:653–660CrossRefGoogle Scholar
  25. Kjellberg F, Doumesche B, Bronstein JL (1988) Longevity of a fig wasp (Blastophaga psenes). Proceed Konink Nederl Akad Wet Ser C Biol Med Sci 91:117–122Google Scholar
  26. Kjellberg F, Gouyon PH, Ibrahim M, Raymond M, Valdeyron G (1987) The stability of the symbiosis between dioecious figs and their pollinators: a study of Ficus carica L. and Blastophaga psenes L. Evolution 41:693–704CrossRefGoogle Scholar
  27. Lambert FR, Marshall AG (1991) Keystone characteristics of bird-dispersed Ficus in a Malaysian lowland rain forest. J Ecol 79:793–809CrossRefGoogle Scholar
  28. Milton K (1991) Leaf change and fruit production in six neotropical Moraceae species. J Ecol 79:1–26CrossRefGoogle Scholar
  29. Milton K, Windsor DM, Morrison DW, Estribi MA (1982) Fruiting phenologies of two netropical Ficus species. Ecology 63:752–762CrossRefGoogle Scholar
  30. 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
  31. Opler PA, Frankie GW, Baker HG (1980) Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 68:167–188CrossRefGoogle Scholar
  32. Patel A (1996) Variation in a mutualism: phenology and the maintenance of gynodioecy in two Indian fig species. J Ecol 84:667–680CrossRefGoogle Scholar
  33. Patel A (1997) Phenological patterns of Ficus in relation to other forest trees in southern India. J Trop Ecol 13:681–695CrossRefGoogle Scholar
  34. Pereira RAS, Semir J, Menezes AO (2000) Pollination and other biotic interactions in figs of Ficus eximia Schott (Moraceae). Braz J Bot 23:217–224Google Scholar
  35. Putz FE, Romano GB, Holbrook NM (1995) Comparative phenology of epiphytic and tree-phase strangler figs in a Venezuelan palm savanna. Biotropica 27:183–189CrossRefGoogle Scholar
  36. Pyper BJ, Peterman RM (1998) Comparison of methods to account for autocorrelation in correlation analyses of fish data. Can J Fish Aquat Sci 55:2127–2140CrossRefGoogle Scholar
  37. Ragusa-Netto J (2002) Fruiting phenology and consumption by birds in Ficus calyptroceras (Miq.) Miq. (Moraceae). Braz J Biol 62:339–346PubMedGoogle Scholar
  38. Ramírez BW (1974) Coevolution of Ficus and Agaonidae. Ann Miss Bot Garden 61:770–780CrossRefGoogle Scholar
  39. Rasmussen PW, Heisey DM, Nordheim EV, Frost TM (1993) Time-series intervention analysis: unreplicated large-scale experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 138–158Google Scholar
  40. Reich PB, Borchert R (1984) Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J Ecol 72:61–74CrossRefGoogle Scholar
  41. Rolim GS, Sentelhas PC, Barbieri V (1998) Planilhas no ambiente EXCELTM para os cálculos de balanços hídricos: normal, sequencial, de cultura e de produtividade real e potencial. Rev Bras Agrometeorol 6:133–137Google Scholar
  42. Shanahan M, Compton SG, So S, Corlett R (2001a) Fig-eating by vertebrate frugivores: a global review. Biol Rev 76:529–572Google Scholar
  43. Shanahan M, Harrison RD, Yamamura N, Boen W, Thornton IWB (2001b) Colonization of an island volcano, Long Island, Papua New Guinea, and an emergent island, Motmot, in its caldera lake. V. Colonization by figs (Ficus spp.), their dispersers and pollinators. J Biogeogr 28:1365–1377CrossRefGoogle Scholar
  44. Spencer H, Weiblen GD, Flick B (1996) Phenology of Ficus variegata in a seasonal wet tropical forest at Cape Tribulation, Australia. J Biogeogr 23:467–475CrossRefGoogle Scholar
  45. Talora DC, Morellato PC (2000) Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Braz J Bot 23:13–26Google Scholar
  46. Terborgh J (1986) Keystone plant resources in the tropical forest. In: Saulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 330–344Google Scholar
  47. Thornthwaite CW, Mather JR (1955) The water balance. Laboratory of Climatology, New JerseyGoogle Scholar
  48. Thornton IWB, Compton SG, Wilson CN (1996) The role of animals in the colonization of the Krakatau Islands by fig trees (Ficus species). J Biogeogr 23:577–592CrossRefGoogle Scholar
  49. Thornton IWB, Cook S, Edwards JS, Harrison RD, Schipper C, Shanahan M, Singadan R, Yamuna R (2001) Colonization of an island volcano, Long Island, Papua New Guinea, and an emergent island, Motmot, in its caldera lake. VII. Overview and discussion. J Biogeogr 28:1389–1408CrossRefGoogle Scholar
  50. Tweheyo M, Lye KA (2003) Phenology of figs in Budongo forest Uganda and its importance for the chimpanzee diet. Afr J Ecol 41:306–316CrossRefGoogle Scholar
  51. Venables WN, Ripley BD (1999) Modern applied statistics with S-PLUS. Springer-Verlag, New YorkGoogle Scholar
  52. Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol 47:299–330CrossRefPubMedGoogle Scholar
  53. Wharton RA, Tilson JW, Tilson RL (1980) Asynchrony in a wild population of Ficus sycomorus. S Afr J Sci 76:478–480Google Scholar
  54. Windsor DM, Morrison DW, Estribi MA, De Leon B (1989) Phenology of fruit and leaf production by “strangler” figs on Barro Colorado Island, Panama. Experientia 45:647–653CrossRefGoogle Scholar
  55. Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18Google Scholar
  56. Wolf JHD (1994) Factors controlling the distribution of vascular and non-vascular epiphytes in the northern Andes. Vegetatio 112:15–28CrossRefGoogle Scholar
  57. Wright SJ (1996) Phenological responses to seasonality in tropical forest plants. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Kluwer Academic Publishers, Boston, pp 440–460Google Scholar
  58. Wright SJ, van Shaik CP (1994) Light and the phenology of tropical trees. Am Nat 143:192–199CrossRefGoogle Scholar
  59. Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Rodrigo Augusto Santinelo Pereira
    • 1
  • Efraim Rodrigues
    • 2
  • Ayres de Oliveira MenezesJr
    • 2
  1. 1.Depto de BiologiaFFCLRP–USPRibeirão PretoBrazil
  2. 2.Depto de AgronomiaCCA–UELLondrinaBrazil

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