Plant Ecology 173: 203–213, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.
203
Phenological patterns among plant life-forms in a subtropical forest in southern Brazil Márcia C. M. Marques*, James J. Roper and Ana Paula Baggio Salvalaggio Departamento de Botânica, SCB, Universidade Federal do Paraná, Caixa Postal 19031, 81531-970 Curitiba, Paraná, Brasil; *Author for correspondence (e-mail:
[email protected]) Received 14 January 2003; accepted in revised form 28 May 2003
Key words: Araucaria angustifolia, Atlantic Rain forest, Daylength, Epiphytes, Flowering, Flushing, Fruiting, Leaf-fall, Lianas, Life-forms, Phenology
Abstract Phenological patterns in tropical plants usually are associated with the clear seasonality of rainfall associated with very different wet and dry seasons. In southern Brazil, in a subtropical forest with no pronounced dry season 共average annual precipitation ⫽ 1389 mm, minimum monthly average c. 75 mm兲, plant phenology was studied to test for patterns 共periodicity兲, to examine how phenological patterns vary among life-forms, and to test whether phenological cycles are associated with climatic variables. Thirty-seven plant species in four life-forms 共trees, shrubs, lianas and epiphytes兲 were studied for 2 yr 共1996-98兲 in an Araucaria forest remnant in southern Brazil, in the state of Paraná. Correlation and multiple regression methods established relationships between phenology and climate in terms of daylength, temperature and rainfall. In this Araucaria forest, plants showed seasonality in most life-forms and phenological phases. Leaf-fall, with its peak during the drier months 共April to July兲, was the most seasonal. Flushing and flowering occurred during the wetter months 共September to December兲, while fruiting occurred all year long. Phenologies varied among life-forms, and were strongly associated with daylength or temperature of preceding months, suggesting that plants receive their phenological cues well in advance of their phenological response. Phenologies in this Araucaria forest appear to be associated with the most predictable and highly correlated of the climatic variables, daylength and temperature and least so with rainfall, which is unpredictable.
Introduction Tropical plants often show temporal phenological patterns 共Frankie et al. 1974; Opler et al. 1980; Lieberman 1982; Kinnaird 1992兲 that are associated with well-defined wet and dry seasons 共Rathcke and Lacey 1985兲. However, seasonality in phenology occurs without well-defined seasonality in rainfall 共Hilty 1980兲, suggesting that other climatic factors may be important in determining phenology. These climatic factors often covary with latitude 共Ter Steege and Persuade 1991兲. Plant phenologies are the result of interactions of biotic and climatic factors that, through natural selection, determine the most efficient
timing for growth and reproduction 共Van Schaik et al. 1993兲. Biotic factors include morphological and physiological adaptations of plants 共Borchert 1983兲, as well as the behaviour of pollinators and seed dispersers 共Van Schaik et al. 1993兲. Climatic factors include photoperiod 共Wright and Van Schaik 1994兲, temperature 共Arroyo et al. 1981兲, and rainfall 共Opler et al. 1976兲. While phenological patterns may be due to several factors 共Lieth 1974兲, understanding phenology in relation to climate is an important first step. Since climatic variables are often highly intercorrelated, testing their influence on phenology requires, firstly, finding significant correlations of phenology with climatic variables 共Smith-Ramírez and Armesto
204 1994; Morellato et al. 2000兲 then, secondly, controlling for interactions among these variables so that the most parsimonious model of the influence of climate on phenology can be derived. Different plant species within a community may share phenological patterns to varying degrees for a variety of reasons. For example, being subject to the same climatic regimes, plant species may share patterns independently of their morphological and physiological adaptations. Also, different species may show similar patterns in phenology because of close phylogeny 共Wright and Calderon 1995兲. On the other hand, different life-forms may respond differently to climatic factors because of morphological and physiological adaptations reflecting different ways in which water and nutrients are sequestered and utilized 共Sarmiento and Monasterio 1983; Smith-Ramirez and Armesto 1994兲. These various considerations have been studied for trees and shrubs in seasonal forests in Latin America 共e.g., Frankie et al. 1974, Morellato et al. 1989, Opler et al. 1980兲, but community-wide patterns with a variety of life-forms, including lianas and epiphytes, are still relatively poorly understood 共see Croat 1975, Morellato and Leitão Filho 1996兲. For two years 共1996-1998兲 the phenology of several species distributed among four life-forms was studied in southern Brazil in a particular type of rain forest. This rain forest is dominated by the endemic species Araucaria angustifolia 共Bertol.兲 Kuntze, and is adjacent to Atlantic Rain Forests with which it shares many floristic features. Araucaria forest lies in a transition zone between tropical and temperate climates and is characterized by rainfall throughout the year and moderate temperatures 共Hueck 1953兲. Since monthly minimum rainfall exceeds 60 mm, this forest may be considered as weakly seasonal with respect to rainfall 共Wright and Van Schaik 1994兲. This forest extended historically into northern Argentina and eastern Paraguay. Araucaria forests occupy only a small fraction of their former range and are rapidly disappearing with the largest contiguous remaining forests currently found in the state of Paraná, in southern Brazil 共e.g., 1.3% in Paraná, Britez et al. 2000兲. Because of the weak seasonality in rainfall and the subtropical latitude 共which lacks the extremes of daylength and temperature typical of higher latitudes兲, the phenology of this Araucaria forest, and its dependence on climate in Paraná, was of interest. The phenology of the plant community was studied to answer the following questions: 共1兲 Do any clear phenologi-
cal patterns exist? If they do, then: 共2兲 are they consistent within and shared amongst life-forms?, and 共3兲 how are they correlated with the important climatic variables?
Methods Study site This study took place in a 50-ha Araucaria forest remnant in eastern Paraná State, southern Brazil 共25° 25' S, 49° 19' W, 900 m altitude兲. This forest fragment is floristically representative of other Araucaria forests found in the region 共Dittrich et al. 1999; C. Kozera, S. M. Silva and V. Dittrich, unpubl. data兲. Climate The climate type is type Cfb of the Köppen classification system, i.e., humid subtropical and mesothermic with mild winters and occasional hard frosts and no pronounced dry season 共Iapar 1978兲. The average monthly temperature ranges from 13 °C 共in June/July兲 to 21 °C 共in February兲. Annual precipitation during the period 1970-95 averaged 1389 mm, with January/ February receiving the greatest rainfall and July/August receiving the least. During the years of this study 共1996-98兲 rainfall was greater 共 ⬎ 1700 mm兲 than that of the average of the preceding 25 yr 共Figure 1兲. Species’ phenology Study species included four life-forms: 13 tree species, seven shrubs, three lianas and 14 epiphytes 共Appendix兲. Plant families followed Cronquist´s classification. Phenology was recorded every c. 15 days from April 1996 to March 1998 共n ⫽ 50兲. Phenology for each individual plant was classified as follows: 共1兲 leaf-fall, 共2兲 flushing, 共3兲 flowering, and 共4兲 fruiting. Leaf fall was defined as when ⬎ 50% of the leaves on the plant showed senescence or fallen leaves were on the ground. Flushing was the interval between when leaf buds began opening to when new leaves were at least 75% of their final size. Flowering 共anthesis兲 was the presence of one or more open flowers. In Araucaria angustifolia and Podocarpus lambertii Klotzsch flowering was when male cones were fully developed and pollen-filled or when female cones appeared. Fruiting was the presence of one or more fruit. Due to the floristic diversity of this forest 共up to
205
Figure 1. Climate during the 2-yr of study 共1996-98兲 of Araucaria forest in southern Brazil, with the 25-yr averages for temperature and rainfall: 共a兲 temperature 共left axis兲 with daylength 共right axis兲; 共b兲 rainfall 共left axis兲 with daylength 共right axis兲; The climate lines for the 25-yr averages are not identical in both years because the points were calculated for the dates at which the phenological samples were gathered, which were not identical in both years. Data of IAPAR 共Agronomic Institute of Paraná兲.
500 species in all life-forms兲, 37 plant species were studied. From five to 10 individuals in each species were selected for study, giving a total sample of 216 individuals, each observed 50 times. The four life-forms were chosen to restrict plants in this study to native, non-herbaceous, species. Individual adult plants were chosen randomly along several trails within the study area. While a minimum of five individuals of each species was selected for study 共following Fournier and Charpentier 1975; the appendix lists species and sample sizes兲, mortality reduced that number in a few cases. Voucher specimens reside in the herbarium of the Botany Department at the Federal University of Paraná 共UPCB兲. Phenological data recorded were the number of species in each life-form exhibiting a phenological phase. Statistical analyses To examine whether plant life-forms share phenological patterns, correlation analysis was used to correlate the four phenological phases among life-forms. Correlation analysis was also used to test for the re-
lationship between phenological patterns and climate. Monthly lags in climate were introduced so that phenology could be correlated with climate at earlier months varying from the current date up to 6 mo before the current date. All of the five variables 共daylength, rainfall 2 yr and 25 yr and temperature 2 yr and 25 yr兲, and their respective five lag times 共for a total of 25 variables兲, were correlated with each of the four phenological phases. In this way, the lag time giving the greatest correlation coefficient indicated the approximate interval 共in months兲 between climate effect and plant response. To test the importance of all climatic variables together, multiple regression analysis was used. Stepwise regression with the mixed selection routine was used, including in the model all five climatic variables 共independent variables兲 at the lag time that was shown to have the greatest correlation with the phenological phases 共dependent variables, see correlations above兲. In this way, the final resulting models contained the variable or combination of variables that best explained the relationship between these climatic variables and each of the four phenological phases.
Results Phenology in Araucaria forest In this Araucaria forest, plants showed seasonal phenological patterns 共Figure 2兲. Correlations between life-forms for different phenological patterns demonstrated that life-forms often showed similar patterns 共Figure 3, Figure 4, Table 1兲. Leaf-fall was the most strongly seasonal among the phenological variables in the Araucaria forest. The peak is during the months of least rainfall, from April to July, and is common among life-forms except epiphytes 共Figure 3, Table 1兲. Flushing in trees and lianas is also seasonal, but less so, and occurs mostly between September and November, during the wettest part of the year 共Figure 3, Table 1兲. Shrubs and epiphytes, on the other hand, while correlated with each other 共Table 1兲, do not show an obvious flushing cycle 共Figure 3兲. Flowering, which follows flushing, peaks between September and December, is also seasonal. Again epiphytes are the least obviously seasonal life-forms 共Figure 4兲, and are the least correlated with other life-forms 共Table 1兲. Fruiting, is less seasonal, and fruiting may be observed year round for many species. Correla-
206
Figure 2. Overall phenological patterns 共all study species together兲 occurring in the Araucaria forest in southern Brazil in 1996-98: 共a兲 leaf-fall and flushing, and 共b兲 flowering and fruiting. Arrows indicate vernal 共filled兲 and autumnal 共open兲 equinoxes 共in the southern hemisphere兲.
tions between shrubs and lianas, and lianas and epiphytes show that they somewhat share fruiting patterns 共r ⫽ 0.40 and 0.46 respectively, Figure 4, Table 1兲. Relationships between phenology and climate Monthly average temperature, rainfall and daylength were all correlated 共all r ⬎ 0.45, n ⫽ 50, P ⬍ 0.05兲. Long-term average monthly temperature 共r ⫽ 0.96兲 and average monthly precipitation 共r ⫽ 0.85兲 were most strongly correlated with daylength of the previous month. For the short-term, the correlation between temperature and daylength remained high 共r ⫽ 0.93兲, while the correlation between rainfall and daylength was lower 共r ⫽ 0.58兲 with no lag time. Thus, climate shows seasonal patterns, with rainfall being the least predictable, temperature very predictable and daylength perfectly predictable 共being an astronomical phenomenon, Figure 1兲. Daylength and temperature are so strongly correlated 共r ⱖ 0.93, after a 1-mo lag兲 that they cannot both be used in re-
gression analysis because of multicollinearity 共Neter et al. 1985兲. With such high correlations, one variable may be substituted for the other without loss of information. Therefore we use daylength/temperature in the Discussion, to emphasize that they must be considered as a single variable, with a 1-mo lag-time in temperature. Regression analysis showed the very consistent trend in that daylength/temperature was uniformly the most important of the climatic variables associated with phenology 共Table 2兲. Daylength/temperature in the regressions explained from 31 to 66% of the variation in phenology in all life-forms. Exceptions are flushing and flowering in epiphytes, and fruiting in shrubs, which were least associated with climate 共all r2 ⬍ 0.15兲. Also, in lianas only 25% of the variation in fruiting was explained by daylength/temperature and precipitation 共Table 2兲. While daylength/temperature was important in regressions, the number of months varied by phenological phase and life-form. In general, phenological phases were most strongly associated with daylength/temperature with a lag of 4-5 mo 共Table 2兲. Precipitation was important in combination 共but not interacting兲 with daylength/ temperature in leaf-fall in trees 共r2 ⫽ 0.44兲. Precipitation in combination with daylength/temperature was marginally important for flowering and fruiting in lianas 共r2 ⫽ 0.46 and r2 ⫽ 0.25, respectively兲. Except for trees, flushing and flowering increased in all lifeforms while daylength/temperature declined, as shown by the negative regression coefficients, while fruiting and leaf-fall increased with increasing daylength/temperature, except for fruiting in shrubs 共Table 2兲. In only three cases were the r2 values ⬍ 0.25: for flushing and flowering in epiphytes and fruiting in shrubs.
Discussion This Araucaria forest is truly seasonal in most phenological events, which are consistent within lifeforms, but not always among life-forms. Phenology is partly explained by two climatic variables, daylength and temperature. The subtropical location and the influence of tropical and temperate floras 共Leite 1994兲 may provide the information that will help to understand the rest of the variation in phenology in this Araucaria forest. Leaf-fall is the most seasonal phase in the Araucaria forest, and is restricted to the months of lowest
207
Figure 3. Phenological patterns for four life-forms in the Araucaria forest in southern Brazil: 共a-d兲 leaf-fall, and 共e-g兲 flushing.
rainfall, and in all life-forms comes 3-5 mo after the peak in daylength/temperature. Leaf-fall in tropical forests often is associated with dry seasons 共Frankie et al. 1974; but see Wright and Cornejo 1990兲, while in some cases daylength and tempera-
ture may be more important 共Lieberman and Lieberman 1984; Morellato et al. 1989兲. Leaf-fall in the Araucaria forest is most strongly associated with daylength/temperature 共r2 between 0.44 and 0.58, Table 2, Table A1兲, and only in trees, in combina-
208
Figure 4. Phenological patterns for four life-forms in the Araucaria forest in southern Brazil: 共a-d兲 flowering, and 共e-g兲 fruiting.
tion with rainfall. Frosts, when they do occur, are most frequent from May to August. Temperatures just under 10 °C can cause plant injury 共Longman and Jeník 1987兲 and so temperature 共and frosts, but only
during the same time period兲 may explain a part of the variation in leaf-fall. While leaf-fall is most strongly associated with daylength/temperature of 3-5 mo prior, interestingly, the transition from declining
209 Table 1. Correlations among four plant life-forms during each of four phenological phases, demonstrating that different life-forms may share phenological patterns in a weakly seasonal Araucaria forest in southern Brazil. Phenological phase
Life-form
Shrubs
Lianas
Epiphytes
Leaf fall
Trees Shrubs Lianas Trees Shrubs Lianas Trees Shrubs Lianas Trees Shrubs Lianas
0.73 **
0.45 ** 0.70 **
ns
0.35 * 0.37 *
0.51 **
0.62 ** 0.56 **
ns
ns 0.40 *
0.50 0.63 0.64 0.28 0.46 ns 0.36 ns ns ns ns 0.46
Flushing
Flowering
Fruiting
** ** ** * ** *
**
*P ⬍ 0.05, **P ⬍ 0.01, ns – P ⬎ 0.05, n ⫽ 50.
to increasing number of species exhibiting leaf fall occurs at the vernal equinox. In tropical studies it has been shown that phenological patterns change at the equinox, often with less than 30 min change in daylength 共Rivera and Borchert 2001兲. If this is the stimulus, it is interesting that one effect of this trigger is the synchrony with daylength in previous months 共Figure 1, Figure 2兲. Flushing and leaf-fall are often correlated in intensity and timing in which flushing follows after leaffall 共Morellato et al. 1989兲. In Araucaria forest flushing showed less seasonality, and was only correlated with leaf-fall in trees and shrubs 共Table 1兲. Regression with daylength/temperature 共the only significant variable兲 had lower r2 values than leaf-fall. New leaf production is continuous in many species here, even in those with a marked seasonal leaf-fall. Also, several species show seasonality in leaf production, and so the forest contains a mix of both leaf-producing tendencies. Flowering and flushing may overlap in some species given that the same meristems that produce buds also produce flowers 共Borchert 1983兲. However, this was observed only in lianas and shrubs. Flowering, in both seasonal and aseasonal forests, often occurs in the transition between drier and wetter periods 共Frankie et al. 1974; Morellato et al. 1989; Talora and Morellato 2000兲 while in some aseasonal systems flowering may occur throughout the year 共Hilty 1980兲. In the Araucaria forest flowering was concentrated during September and October but can occur at any time of the year. Synchronous flowering may be
due to seasonally active pollinators, or because several species share the same set of pollinators, while asynchronous flowering may reduce competition for pollinators 共Rathcke and Lacey 1985; Van Schaik et al. 1993兲. This study was not designed to determine this relationship. Further research on the interactions between pollinators and plant species is warranted to elucidate the reasons for variability in timing of flowering. Fruiting year-round in the Araucaria forest follows the tendency of many tropical forests 共Frankie et al. 1974; Hilty 1980; Talora and Morellato 2000兲. Here, while the peak of fruiting follows after that of flowering, fruit are found throughout the year, and correlations with climate variables were relatively low. In animal-dispersed plants, year-round fruit availability may be a plant strategy to reduce competition among plants for dispersers 共Snow 1965兲. Fruiting in the least wet part of the year may favour seed dispersal of anemochoric fruits 共mostly epiphytes and lianas兲 in the Araucaria forest. It has been suggested that tropical-tree phenology may be associated with equinoxes 共Rivera and Borchert 2001兲. In this study, only leaf-fall appeared to have a close association 共transition from declining to increasing兲 with the southern Vernal Equinox 共Figure 2兲. Interestingly, equinoxes occurred during peaks and troughs of the number of species flowering and fruiting 共Figure 2兲. Yet, if the equinoxes are triggers, then, rather than occur at the equinox, phenology should follow the equinox by the amount of time the plant requires to respond to the trigger. Thus, the influence of the equinoxes remains to be tested, perhaps by examining the timing of the equinox with respect to that of the release of the inducers of the phenological phase in question. Phenological differences among life-forms With the exception of leaf fall and flowering life-forms presented different phenological patterns 共low correlations, Table 1, lag times, Table 2兲. Different patterns in each life-form may be due to different rooting systems and the resultant differences in resource requirements, availability, and storage capabilities among others. In savannas, for example, timing of reproduction in trees, shrubs and herbs was different for each group and was associated with root depth 共Sarmiento and Monasterio 1983兲. Light regimes also vary greatly for each life-form due to stratification of the forest 共Larcher 2000兲, which may
210 Table 2. Regression models of the relationships between phenology and climate 共daylength/temperature1, precipitation兲 for Araucaria forest. Significant relationships 共P ⬍ 0.05兲 are shown, except in two cases 共*兲 where 0.08 ⬎ P ⬎ 0.05. 共r2, without this marginally important variable, is shown in parenthesis兲. Phenological Phase
Life-form
Independent variables
Leaf-fall
Trees Shrubs Lianas Epiphytes Trees Shrubs Lianas Epiphytes Trees Shrubs Lianas Epiphytes Trees Shrubs Lianas Epiphytes
D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T D/T
Flushing
Flowering
Fruiting
共lag in months,sign of regression coefficient兲 共5, 共4, 共4, 共3, 共0, 共5, 共5, 共3, 共5, 共4, 共5, 共5, 共2, 共6, 共3, 共4,
⫹兲 and Precipitation 共6, ⫹兲 ⫹兲 ⫹兲 ⫹兲 ⫹兲 ⫺兲 ⫺兲 ⫺兲 ⫺兲 ⫺兲 ⫺ 兲 and 25 yr Precipitation* 共5, ⫺ 兲 ⫺ 兲 or Precipitation 共6, ⫺ 兲 ⫹兲 ⫺ 兲 or 25 yr Precipitation 共5, ⫺ 兲 ⫹兲 and Precipitation *共5, ⫹兲 ⫹兲
r2 0.44 0.56 0.44 0.58 0.31 0.42 0.36 0.14 0.66 0.38 0.46 0.13 0.36 0.09 0.24 0.48
共0.41兲 or 0.14 or 0.10 共0.19兲
1
D/T indicates daylength and 1-mo lagged temperature. Because of strong correlations these variables must be viewed as being inseparably linked: i.e., they cannot be analysed separately due to multicollinearity 共see text兲.
translate to different microclimates and result in different phenological timing patterns. Phenology and climate The alternation of dry and wet periods is often associated with tropical phenological cycles 共Opler et al. 1976; Wright 1991兲. When moving away from the equator phenological patterns should be more influenced by daylength and temperature 共which became more variable兲 and less by rainfall 共Alvim 1967; Rivera and Borchert 2001兲. Daylength and solar elevation 共latitude兲 determine the light and temperature regimes that influence plant primary production 共Van Schaik et al. 1993; Wright and Van Schaik 1994兲. In this sub-tropical location, the 3-hr annual variation in photoperiod is greater than that in the tropics 共Longman and Jeník 1987兲 and in the Araucaria forest it is apparently an important influence in the phenology of most plant species. Also, because daylength and temperature in the preceding month are so strongly correlated, it is impossible to determine which one is most important without experimental work. Regardless, daylength and temperature cycles are so strong and fixed that they offer consistent information regarding the annual cycle in this region. Daylength
can be important for various aspects of timing in plant cycles, such as leaf-fall 共Alvim 1967; Longman and Jenik 1987; Morellato et al. 1989兲, flowering 共Ter Steege and Persuad 1991兲, and dormancy breaking 共Njoku 1963; Rivera and Borchert 2001兲. In the Araucaria forest all phenological phases were associated with daylength/temperature. Rain, on the other hand, may vary greatly and is therefore not a good predictor of the annual cycle. If water is not limiting, then plants would not be expected to select for cues in rainfall as it is much less reliable in comparison to daylength or temperature.
Acknowledgments Thanks to S.M. Silva for plant identification, and to M. Bündchen and S. Ribas for their help in the field. Thanks to the Prefecture of the Municipality of Curitiba for permission to carry out this research in Barigüi Park. The editorial suggestions of Dr. D. M. Newbery were very much appreciated. The Research Support Program of the Federal University of Paraná provided support. A. P. B. Salvallaggio received support from the program Iniciação Científica at the Federal University of Paraná.
211 Appendix Table A1. Plant life-form, number of individuals 共n兲 and phenology 共months when each phenological phases was recorded over 2-yr兲 of 37 species of the Araucaria forest, southern Brazil. C ⫽ continuous; * deciduous species, ** annual species. Family / Species Anacardiaceae Schinus terebinthifolius Raddi Araceae Philodendron sp. Araucariaceae Araucaria angustifolia 共Bertol.兲 Kuntze 共乆兲 Araucaria angustifolia 共Bertol.兲 Kuntze 共么兲 Bignoniaceae Pithecoctenium crucigerum 共L.兲 A. H. Gentry Bromeliaceae Aechmea distichanta Lem. Aechmea recurvata 共Klotzch兲 L.B.Sm. Bilbergia nutans H. Wendl.
Life form
n
Plant phenology Leaf-fall Flushing
Flowering
Fruiting
C
C
C
10 C
C
Sep-Mar
Jan-Feb
Tree Tree
5 C 4 C
C C
C C
Apr-Jul –
Liana
5 Apr-Sep*
Sep-Mar
Oct-Dec
Feb-Sep
Sep-Dec Oct-Jun Jan-Feb, May-Sep Dec-Jan
Oct-Jan Jan-Jul Mar, Jun-Oct
Dec-Jul Feb-Jun
Tree Epiphyte
7 Jan-Sep
Epiphyte Epiphyte Epiphyte
8 Feb-Aug 10 C 4 Oct-Nov
May-Aug Feb-Sep Apr-Jul
Vriesea friburgensis Mez**
Epiphyte
10 C
Apr-Jun, Nov-Jan
Cactaceae Hatiora salicornioides Britton and Rose Lepismium cruciforme 共Vell.兲 Miq.
Epiphyte Epiphyte
7 May-Aug 5 Dec-Sep
Aug-Nov Aug-Oct
Epiphyte
9 C
Jul-Nov
Sep-Nov Jul-Aug, Oct-Nov Jun-Dec
Tree
5 Feb-Aug
C
⫺
⫺
Tree
5 Jan, Mar-Sep*
Aug-Feb, Apr
Sep-Oct
Oct-Jan
Epiphyte
6 Nov-Aug*
Jan-Oct
Sep-Nov
Sep-Dec
Tree Tree Tree
8 C 3 C 5 C
Aug-May Oct-May Aug-Apr
Oct-Dec Nov-Feb Aug-Jan
Dec-Apr Dec Dec-Jan
Shrub
4 Oct-Jul
C
C
C
Liana
1 May-Jun
Jul-Mar
Nov-Jan
Feb-Sep
Shrub
4 Jan-Jul
Jun-Mar
Aug-Oct
Sep-Jun
Tree
Aug-Apr
Dec-Apr
Mar-May
Tree Shrub Tree
5 Apr-Aug, Oct-Dec 5 May-Aug* 5 Dec-Aug 5 Feb-Jul
Aug-Nov C C
Oct-Nov Oct-Dec Nov-Feb
Dec Aug-Sep Mar-Apr
Epiphyte
4 ⫺
Jan-Jun
Feb-Nov
Epiphyte Epiphyte
5 ⫺ 5 C
May-Aug, Nov-Dec Jan Jul-Jan
Apr-Jul Jan-Jun
⫺ Mar-Jun
Liana
4 Jan-May*
C
Sep-Nov
Dec-Mar
Epiphyte Epiphyte
5 Nov-May 4 Feb-Apr
Sep-Jan C
C Oct-Jul
C Jan-Sep
Lepismium houlletianum 共Lem.兲 Barthlott Canellaceae Capsicodendron dinisii 共Schwacke兲 Occhioni Flacourtiaceae Casearia decandra Jacq. Gesneriaceae Sinningia douglasii 共Lindl.兲 Chautems Lauraceae Cryptocarya aschersoniana Mez Ocotea corymbosa (Meisn.) Mez Ocotea puberula Nees Malvaceae Pavonia malvacea 共Vell.兲 Krapov. and Cristóbal Mimosaceae Bauhinia microsthachia 共Raddi兲 J. F. Macbr. Monimiaceae Mollinedia clavigera Tul. Myrtaceae Eugenia prismatica Legrand Eugenia uniflora L. Myrceugenia ovata var. gracilis 共Burret兲 Landrum Myrcia hatschbachii Legrand Orchidaceae Campylocentrum aromaticum Barb. Rodr. Leptotes unicolor Barb. Rodr. Pleurothalis luteola Lindl. Passifloraceae Passiflora actinia Hooker Piperaceae Peperomia catharinae Miq.** Peperomia tetraphylla 共G. Forst兲 Hook. and Arn.
Jan-Oct
Aug-Mar
212 Table A1. Continued. Family / Species Piper gaudichaudianum Kunth var. gaudichaudianum Podocarpaceae Podocarpus lambertii Klotzsch 共乆兲 Podocarpus lambertii Klotzsch 共么兲 Rubiaceae Psychotria suterella Müell. Arg. Rudgea parquioides (Cham.) Müll.Arg. Sapindaceae Allophylus edulis 共A.St.-Hil.兲Radlk. Solanaceae Solanum granuloso-leprosum Dunal Solanum pseudoquina A.St.-Hil.
Life form
n
Plant phenology Leaf-fall Flushing
Flowering
Fruiting
Shrub
3 Mar-Jul
C
Apr-Nov
Apr-Jan
Tree Tree
5 Mar-Aug 4 Feb-Aug
C C
Oct-Jan C
Jan-Jul ⫺
10 Mar-Sep 5 Jan-Jun
C C
Feb-Apr Dec-Jan, May-Jun
May-Oct Dec-May
Shrub Shrub
Tree
5 Dec-Sep*
Aug-May
Aug-Oct
Nov-Dec
Tree Shrub
7 Oct-Jul 5 Dec-Oct
C C
Jun-Dec Dec-Apr
Jul-Jan Aug-Jan
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