Electronic supplementary material
Continental-scale patterns of Cecropia reproductive phenology: Evidence from herbarium specimens
Paul-Camilo Zalamea*, François Munoz, Pablo R. Stevenson, C. E. Timothy Paine, Carolina Sarmiento, Daniel Sabatier and Patrick Heuret
*To whom correspondence should be addressed. e-mail:
Appendix S1: Performance of the randomization test.
We simulated phenological patterns with varying numbers of herbarium specimens to evaluate the performance of the randomization test to detectannualpatterns. We accordingly simulated two datasets, the first made of samples drawn from random data distributed over 12 months, and the second one made of samples drawnfrom data with annual periodicity.
Figure S1 shows the probability of detecting an annual pattern for each simulated dataset. The probability of detecting an annual pattern when the actual pattern is random (first dataset) was about 5%, regardless of sample size (figure S1a). The probability of detecting an annual pattern increased with the sample size (figure S1b). This analysis showed that 15 herbarium specimens is still a low sample size for detecting an annual periodic pattern, but at the same time, if an annual pattern is detected using a low number of collections, the probabilityof misinterpretation is very low. Hence, annual patterns detected from 15 herbarium samples are likely to be true, but we might detect only a subsample of the total annual patterns.
Figure S1 Probability of detecting an annual pattern for (a) simulated random distributed data (the black line represents the 5% limit) and (b) simulated annual data (the black lines represent the 95% and 100% limits).
Appendix S2: The annual component and its corresponding phase in the Fourier spectrum.
If significant, the amplitude of the 12-month component provided in a Fourier spectrum, displays an annual trend in phenology, that is, a single annual alternation of a flowering season (i.e., numerous observations of flowering data) and of a vegetative season(i.e., few or no observations). Figure S2a shows an example of the annual component obtained for C. sciadophylla in the Guiana Shield region. Other components of shorter periods represent, respectively, two alternations per year (6-month period), three alternations per year (4-month period), and so on. If the annual component was clearly predominant against the others, the corresponding phase yielded the position (i.e., month) of the flowering peak within a year (figure S2b).
Figure S2 (a)Frequency of herbarium collections by month (bars) and annual periodic pattern provided in the Fourier spectrum for the first component (black line), for C. sciadophylla in the Guiana Shield region (n = 40). (b) The phase between two annual components represents the lag between their peaks. Here, the flowering peak (dashed line) occurs around October 1st and is associated to a -3 months phase, that is, it occurs 3 months before the reference peak (i.e., January 1st, solid line).
Table S1 Flowering peaks and timing of flowering production between reproductive peaks and the peaks of climatic variables (i.e., precipitation and median temperature) for species-region combinations with significant annual patterns.
FloweringRegion / Species / Peak / Prec. Lag / Temp. Lag
Andes and Central America mountains (climatic region i)
C. mutisiana / Mar / 3.5 mo after / 0.5 mo before
C. obtusifolia / Mar / 5.5 mo before / 2 mo before
C. strigosa / Dec / 1.5 mo before / 0.5 mo before
Dry Central America and Caribbean (climatic region ii)
C. obtusifolia / Apr / 4 mo before / 2.5 mo before
C. peltata / Jul / 1 mo before / 0.5 mo after
C. schreberiana / Apr / 3.5 mo before / 3 mo before
Humid Central America andOrinoquía (climatic region iii)
C. insignis / Mar / 5.5 mo before / 2 mo before
C. peltata / Jun / 2 mo before / 0.5 mo after
Western Amazonia (climatic region iv)
C. distachya / Oct / 6 mo before / 2 mo after
Southern Amazonia (climatic region v)
C. engleriana / May / 5 mo before / 5 mo before
C. utcubambana / Aug / 5 mo after / 5 mo after
C. concolor / Nov / 2 mo after / 1.5 mo after
C. polystachya / Nov / 1.5 mo after / 1 mo after
Guiana Shield (climatic region vi)
C. obtusa / Sep / 5 mo before / same mo
C. palmata / Oct / 5 mo before / 1 mo after
C. sciadophylla / Oct / 5.5 mo before / 1 mo after
Caatinga and Cerrado (climatic region vii)
C. pachystachya / Dec / 3.5 mo after / 0.5 mo before
C. saxatilis / Feb / 1 mo before / 4 mo before
Appendix S3: References on Cecropia phenology.
[1] Hilty, S. L. 1980 Flowering and fruiting periodicity in a premontane rain forest in pacific Colombia. Biotropica 12, 292–306.
[2] Roldan, A. I. & Larrea, D. M. 2003 Fenología de 14 especies arbóreas y socorras de un bosque yungeño en Bolivia. Ecol Boliv38, 125–140.
[3] Paton, S. 2003 C. obtusifolia and C. insignis timeseries. [online]. Accesed trough
[4] Frankie, G. W., Baker, H. G. & Opler, P. A. 1974 Comparative phenological studies of trees in tropical wet and dry forest in the lowlands of Costa Rica. J. Ecol.62, 881–919.
[5] Fleming, T. H. & Williams, C. F. 1990 Phenology, seed dispersal, and recruitment in Cecropia peltata (Moraceae) in Costa Rican tropical dry forest. J. Trop. Ecol.6, 163–178.
[6] Zimmerman, J. K., Wright. S. J., Calderón. O., Pagan, M. A. & Paton, S. 2007 Flowering and fruiting phenologies of seasonal and aseasonal Neotropical forests: The role of annual changes in irradiance. J. Trop. Ecol. 23, 231–251.
[7] Brokaw, N. V. L. 1998 Cecropia schreberiana in the Luquillo Mountains of Puerto Rico. Bot. Rev.64, 91–120.
[8] Newell, E. A., Mulkey, S. S. & Wright, S. J. 2002 Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia131, 333–342.
[9] O'Brien J. J., Oberbauer, S. F., Clark, D. B. Clark, D. A. 2008 Phenology and Stem Diameter Increment Seasonality in a Costa Rican Wet Tropical Forest. Biotropica40, 151–159.
[10] Milton, K. 1991 Leaf change and fruit production in six neotropical Moraceae species. J. Ecol. 79, 1–26.
[11] Zalamea, P. C., Stevenson, P. R., Madriñán, S., Aubert, P. M. & Heuret, P. 2008 Growth pattern and age determination for Cecropia sciadophylla (Urticaceae). Am. J. Bot.95, 263–275.
[12] Stevenson, P. R. 2004 Phenological patterns of woody vegetation at Tinigua Park Colombia: Methodological comparisons with emphasis on fruit production. Caldasia 26, 125–150.
[13] Cortés, A. I. 2005 Análisis de los patrones de floración de las especies del Parque Tinigua, Colombia. B.Sc. thesis, Universidad de los Andes, Bogotá: Colombia.
[14] Justiniano, M. J. & Fredericksen, T. S. 2000 Phenology of Tree Species in Bolivian Dry Forests. Biotropica32, 276–281.
[15] Bentos, T. V., Mesquita, R. C. G. & Williamson, G. B. 2008 Reproductive Phenology of Central Amazon Pioneer Trees. Trop. Conserv. Sci.1, 186–203.
[16] Wittmann, F. & Parolin, P. 1999 Phenology of six tree species from Amazonia varzea. Ecotropica5, 51–57.
[17] Parolin, P. 2002 Life history and environment of Cecropia latiloba in Amazonian floodplains. Revi. Biol. Trop.50, 531–545.
[18]Schöngart, J., Piedade, M. T. F., Ludwigshausen, S., Horna, V. Worbes,M. 2002 Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests. J. Trop. Ecol.18, 581–597.
[19] Heuret, P. 2002. Analyse et modelisation de sequences d’événements botaniques: applications à la compréhension de la régularité d’expression des processus de croissance, de ramification et de floraison.PhD thesis. Université Henri Poincaré – Nancy I, Nancy: France.
[20] Charles-Dominique, P. 1986 Inter-relations between frugivorous vertebrates and pioneer plants: Cecropia, birds and bats in French Guiana. In Frugivores and seed dispersal (ed. A. Estrada & T. H. Fleming) pp. 119–135. Dordrecht, The Netherlands: Dr. W. Junk Publishers.
[21] Toriola, D. 1998 Fruiting of a 19-year old secondary forest in French Guiana. J. Trop. Ecol.14, 373–379.
[22] Mikich, S. & Silva, S. 2001 Composição floristica e fenologia das espécies zoocoricas de remanescentes de floresta estacional semidecidual no centro-oeste do Parana, Brasil. Acta Bot. Bras.15, 89–113.
[23] Grombone-Guaratini, M. T. & R. R. Rodrigues. 2002. Seed bank and seed rain in a seasonal semi-deciduous forest in south-eastern Brazil. J. Trop. Ecol.18, 759–774.
[24] Ferraz, I. & Micheletto, F. 2001 Germination of seeds of tropical pioneer species under controlled and natural conditions. Rev. Bras. Bot.24, 79–84.
[25] Ferraz, D. K., Artes, R., Mantovani, W. & Magalhães, L. M. 1999 Fenologia de arbores em gragmento de mata em São Paulo, SP. Rev. Bras. Biol.59, 305–317.