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Reproductive phenology of coastal plain Atlantic forest vegetation:
Comparisons from seashore to foothills
Article  in  International Journal of Biometeorology · August 2011
DOI: 10.1007/s00484-011-0482-x · Source: PubMed
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ORIGINAL PAPER
Reproductive phenology of coastal plain Atlantic forest
vegetation: comparisons from seashore to foothills
Vanessa Graziele Staggemeier &
Leonor Patrícia Cerdeira Morellato
Received: 1 December 2010 /Revised: 19 July 2011 /Accepted: 22 July 2011 /Published online: 9 August 2011
# ISB 2011
Abstract The diversity of tropical forest plant phenology has
called the attention of researchers for a long time.We continue
investigating the factors that drive phenological diversity on a
wide scale, but we are unaware of the variation of plant
reproductive phenology at a fine spatial scale despite the high
spatial variation in species composition and abundance in
tropical rainforests. We addressed fine scale variability by
investigating the reproductive phenology of three contiguous
vegetations across the Atlantic rainforest coastal plain in
Southeastern Brazil. We asked whether the vegetations
differed in composition and abundance of species, the micro-
environmental conditions and the reproductive phenology,
and how their phenology is related to regional and local
microenvironmental factors. The study was conducted from
September 2007 to August 2009 at three contiguous sites: (1)
seashore dominated by scrub vegetation, (2) intermediary
covered by restinga forest and (3) foothills covered by restinga
pre-montane transitional forest. We conducted the micro-
environmental, plant and phenological survey within 30
transects of 25 m×4 m (10 per site). We detected significant
differences in floristic, microenvironment and reproductive
phenology among the three vegetations. The microenviron-
ment determines the spatial diversity observed in the structure
and composition of the flora, which in turn determines the
distinctive flowering and fruiting peaks of each vegetation
(phenological diversity). There was an exchange of species
providing flowers and fruits across the vegetation complex.
We conclude that plant reproductive patterns as described in
most phenological studies (without concern about the micro-
environmental variation) may conceal the fine scale temporal
phenological diversity of highly diverse tropical vegetation.
This phenological diversity should be taken into account
when generating sensor-derived phenologies and when trying
to understand tropical vegetation responses to environmental
changes.
Keywords Microenvironmental factors . Phenological
diversity . Resource availability . Seasonality . Tropical forest
Introduction
The diversity of plant phenology patterns in tropical forests
has called the attention of researchers for a long time
(Morellato et al. 2000; Frankie et al. 1974; Janzen 1967;
Richards 1996). We continue investigating the factors that
drive phenological diversity on a wide scale (Bawa et al.
2003; Sakai 2001; Goulart et al. 2005), but understanding
how species phenology is controlled at a fine spatial scale is
also essential for predicting plant responses to environmen-
tal changes. We have recognized the importance of
environmental factors as the proximate clues shaping
tropical plant phenology, even in less seasonal climates
within the tropics (Morellato et al. 2000; Boulter et al.
Electronic supplementary material The online version of this article
(doi:10.1007/s00484-011-0482-x) contains supplementary material,
which is available to authorized users.
V. G. Staggemeier : L. P. C. Morellato (*)
Departamento de Botânica, Laboratório de Fenologia,
Grupo de Fenologia e Dispersão de Sementes,UNESP - Univ Estadual Paulista,
13.506-900, Rio Claro, SP, Brazil
e-mail: patricia.morellato@gmail.com
Present Address:
V. G. Staggemeier
Departamento de Ecologia, Laboratório de Ecologia Teórica e
Síntese, ICB, Universidade Federal de Goiás,
74001-970, Goiânia, GO, Brazil
Int J Biometeorol (2011) 55:843–854
DOI 10.1007/s00484-011-0482-x
http://dx.doi.org/10.1007/s00484-011-0482-x
2006). However, at a local scale, we are unaware of the
variation of plant reproductive phenology despite the
typical high spatial variation in species composition and
abundance of several tropical rainforests (Hubbell 1979;
Gentry 1988; Condit et al. 2000).
Therefore, it has become more and more crucial to
understand plant phenological variability at a local, fine
spatial scale for at least three reasons. First, when
comparing species or vegetation types at a local spatial
scale we may access how the environmental variability,
which is known to drive plant species occurrence and
distribution (Scudeller et al. 2001; Oliveira-Filho and
Fontes 2000), may affect phenological patterns (Heideman
1989; Bendix et al. 2006). Second, comparing phenological
patterns at a local scale may allow us to detect the variation
in plant species response to local climate and its potential
adaptation to climatic shifts imposed by fragmentation
(Haugaasen and Peres 2005; Camargo et al. 2011) or future
climate changes (Schwartz and Hanes 2010; Rutishauser et
al., unpublished data). Finally, most tropical plant species
rely upon animal vectors for pollination and seed dispersal,
and temporal and spatial variations in flowering and
fruiting phenology strongly affect animals that rely upon
flowers or fruits as a food resource (Wheelwright 1985; van
Schaik et al. 1993; Haugaasen and Peres 2005).
In the present paper, we addressed some of these problems
by investigating the reproductive phenology of three contig-
uous vegetation types occurring across the coastal plain of the
weakly seasonal Atlantic rainforest in Southeastern Brazil.
Specifically, we wanted to determine (1) whether the three
vegetation types, locally referred to as restinga vegetation,
differ in composition, species abundance and local micro-
environmental conditions, (2) whether the reproductive
phenology differs among the three vegetation types, and (3)
how the phenology of these vegetations is related to regional
and local scale environmental factors. We expect that the
floristic diversity, defined as the differences in species
composition and abundance among sites, and the micro-
environmental factors will result in phenological differences
among vegetation types. In addition, we expect that severe
environmental conditions (e.g., extreme temperatures, low
relative humidity and higher light incidence) will lead to a
higher degree of seasonality in plant reproduction. Therefore,
the vegetation under extreme microenvironmental conditions
would also exhibit higher phenological seasonality.
Materials and methods
Study area
The study was conducted in the Parque Estadual da Ilha do
Cardoso (PEIC), Cananéia, São Paulo State, Southeastern
Brazil (47˚54′75″W, 25˚03′88″S) from September 2007 to
August 2009. PEIC is a protected continental island of
15,100 ha covered by Atlantic rainforest vegetation
(Bernardi et al. 2005). The PEIC flora was studied in detail
by Barros et al. (1991), Melo and Mantovani (1994), Pinto
(1998) and Sugiyama (1998). The topography of Cardoso
Island is mainly mountainous in its central portion, with
elevations above 800 meters. Our study was developed
across the Atlantic rainforest coastal plain ranging from sea
level to ten meters in altitude. The vegetation is locally
referred to as restinga (Couto and Cordeiro 2005) and is a
vegetation mosaic, including three vegetation types or
physiognomies (Couto and Cordeiro 2005): the scrub
vegetation, the restinga forest and the restinga pre-
montane transitional forest.
Scrub vegetation Located near the sea, the scrub vegetation
grows on sandy ridges and is dominated by scrubs and
herbaceous plants up to 3 m in height (Fig. S1a in the
Electronic Supplementary Material). There is no canopy
(Fig. S1b), and the stem diameters reach about 3 cm.
Litterfall is almost absent (Fig. S1c), and the substrate is
sandy, dry and in some places water can accumulate during
the rainy season, depending on the depth of the groundwa-
ter. The most common species are Dalbergia ecastaphyl-
lum, Dodonea viscosa, Ternstroemia brasiliensis, Baccharis
trimera, Psidium cattleianum, Myrcia multiflora, Myrsine
guianensis and Gaylussacia brasiliensis.
Restinga forest Located in the central portion of the coastal
plain strip, the restinga forest includes trees up to 15 m in
height (Fig. S2a). The canopy is predominantly closed in
this vegetation (Fig. S2b) but presents some eventual
openings. Treelets and trees are the dominant stratum, and
there is a large number of plants with stem branches from
the base (Fig. S2c). Stem diameter ranges from 12 to
25 cm, with some plants exceeding 40 cm. There is a great
number and diversity of epiphytes, especially bromeliads,
orchids, aroids, ferns, bryophytes and lichens. The continuous
litterfall layer (Fig. S2d) presents a large amount of non-
decomposed leaves. The substrate is sandy and predomi-
nantly from a marine source, but there is occasional sand and
clay deposition from a continental source (Fig. S2e), and
floods occur occasionally in certain areas. The widespread
species here include Eugenia spp., Myrcia spp., Psidium
cattleianum, Clusia criuva, Ternstroemia brasiliensis, Calo-
phyllum brasiliensis and palm species.
Restinga pre-montane transitional forest Of the three types
of vegetation, this is located furthest from the sea; it is the
coastal vegetation growing over drier substrates of conti-
nental origin covered by a thick litterfall and humus layer
(Fig. S3c). The restinga pre-montane transitional forest is
844 Int J Biometeorol (2011) 55:843–854
closer to the foothills, sharing a large number of species
with the contiguous pre-montane Atlantic rainforest. The
distinctive forest physiognomy (Fig. S3a) is characterized
by a closed canopy (Fig. S3b) composed by trees 12–18
meters tall and emergent trees up to 25 meters tall; the tree
diameters range from 15 to 30 cm, reaching up to 40 cm.
The forest presents a high diversity and abundance of
epiphytes, and Psychotria nuda is the most common shrub
species in the understory. The distinctive tree species are
Eugenia cuprea, Marlierea tomentosa, Ocotea spp., Molli-
nedia schottiana and Euterpe edulis.
To facilitate the identification of the three study sites and
their vegetation, hereafter we will name them as follows:
seashore, intermediary and foothills instead of scrub
vegetation, restinga forest and restinga pre-montane transi-
tional forest, respectively.
The climate of PEIC is classified, according to the
Köppen system (Köppen 1923), as subtropical humid (Cfa),
i.e. always wet with no dry season and mean temperature
above 20°C (Fig. S4). The average annual temperature and
rainfall for the normal climate (1956–1985) are 21.3°C and
2248 mm, respectively. A warm and rainy wet season with
monthly rainfall totals over 100 mm occurs from September
to May, and there is a colder, less wet season, from June to
August with less frequent rainfall that may fall below
100 mm/month (Fig. S4). During the study period, the
mean temperatures were around 22.1°C, but the total
rainfall in 2007 and 2008 were below the 30-year average
(1702 mm and 1392 mm, respectively; Fig. 1). The climatic
data for the study period were collected by the city of
Cananéia meteorological station (5 km from the study area)
and were obtained from Centro Integrado de Informações
Agrometeorológicas (CIIAGRO); the 30-year historical
data were obtained from the Oceanographic Institute of
the University of São Paulo (USP). The day-length for 25˚
latitude follows Pereira et al. (2001), with the shortest day
of the year occurring in June (10.45 h) and the longest dayin December (13.54 h).
Plant survey and microenvironmental variables
We established ten transects of 25 m×4 m (total sampling:
0.3 ha) in each vegetation type. The seashore vegetation
transects were established about 500 m from the ocean line
and around 2 km from the intermediary vegetation sample
area and 7 km from the foothills sample area. The transects
in the intermediary and foothill vegetations are about 4 km
from each other.
We sampled microenvironmental variables, performed
the plant floristic survey and made phenological observa-
tions within the transects. We consider as microenviron-
mental variables any environmental factor measured and/or
collected in the transects. The environmental variables
provided by the meteorological station (see above) are
considered to be the general or regional environmental
factors that define the climate at the study area and under
which all the studied vegetation types grow. We collected
the following microenvironmental data: air temperature
(°C), relative humidity (%), and the photosynthetic
active radiation (PAR; μmol.s-1.m-2) at 2 m above the
ground using an automatic HOBO® Micro Station (Onset
Computer Corporation) in the wet and warm (January
2009) and in the less wet and cold (June 2009) seasons to
stress the differences between seasons. We performed six
measurements within 30 sec, at three points in each
transect (at the beginning, middle and end of the transect)
during three consecutive days from 10:00 to 14:00 h. We
utilized the mean of the 18 measurements to represent the
microenvironment at each transect. At the same points, we
also measured the openness of the canopy using a fisheye
lens coupled to a digital camera (Nikon Coolpix 8700) at
1.10 m above the soil and calculated the proportion of
white pixels using Gap Light Analyser 2.0 software
(Frazer et al. 1999).
We used the four microenvironmental variables to run a
principal component analysis (PCA) and to ordinate trans-
ects along n-axes (Manly 2004). If the transects differ
regarding the microenvironment, their position along the
axes must be different for each forest type. The areas were
compared considering transects as replicates, and the
correlation matrix was used to obtain the eigenvectors
because the environmental variables were on different
Fig. 1 Climate and plant reproductive phenology for the study period in
the Atlantic rainforest, Southeastern Brazil. (a) Rainfall, mean temper-
ature from September 2007 to August 2009 at Cananéia and day-length
at 25˚ latitude. (b) Percentage of species (n=106) flowering and fruiting
per month in the study area at Cardoso Island, Southeastern Brazil
Int J Biometeorol (2011) 55:843–854 845
scales. For this analysis, we log-transformed the micro-
environmental data to linearize the relationships. The
significance of the axes was obtained by 10,000 Monte
Carlo randomizations (Manly 2004).
Floristic comparisons
The criterion for sampling the woody plants within trans-
ects differed among sites due to the distinctions in the
vegetation structure: in the seashore, we sampled all shrubs
over 1 m in height; in the intermediary and foothill
vegetations, we sampled all individuals over 15 cm of
circumference at breast height.
We calculated the qualitative floristic similarity between
the three vegetations by applying the index of Jaccard and
the index of Sorensen. Both indices range from 0 (complete
dissimilarity) to 1 (complete similarity) and consider only
the presence or absence of species in the compared sites.
We also compared the sites by taking into account the
abundance of species using the quantitative index of
Sorensen and the Morisita-Horn index.
We applied a detrended correspondence analysis (DCA)
to obtain a simultaneous ordination of sites (transects) and
species. The DCA output is an ordination chart with
information on the similarities in composition and abun-
dance of species in the samples. If the areas differ in
composition and abundance of species, the points repre-
senting the transects will not overlap on the chart. For this
analysis, we transformed (log (x +1)) the abundance data to
linearize the relationships, and the percentage of variance
explained by each axis was obtained based on the
correlation of the distance matrices of the original data
and scores (chi-square distance). For all DCA analyses, the
significance of axes was obtained by means of Monte Carlo
randomizations (Manly 2004).
Finally, to examine the relationship between microenvi-
ronment and species composition we performed a pairwise
comparison using the Mantel test (Legendre and Legendre
1998) between two distance matrices: a microenvironmen-
tal matrix based on the four microenvironmental variables
and a species abundance matrix. The species abundances
were log (x+1) transformed, and we used the Bray-Curtis
distance measure for this floristic matrix. Additionally, we
used a relative Euclidian distance measure for the micro-
environmental matrix because it standardizes variables that
are in different scales. A Monte Carlo test based on 999
random permutations was applied to evaluate the signifi-
cance of the Mantel test.
Phenological sampling and data analyses
We conducted phenological observations of 1,027 individ-
uals (Table S1) at monthly intervals from September 2007
to August 2009 on the following phenophases: flower buds,
flowers (anthesis or flowering), immature fruits and mature
fruits (fruits prepared for dispersal or fruiting). We
estimated the intensity of each phenophase using a semi-
quantitative index of intensity ranging from 0 (absence) to
4, with a 25% interval between each presence class 1 to 4
(Fournier 1974). Additionally, we estimated the production
of mature flesh fruits by directly counting the fruits of each
plant to have a more accurate definition of the peak of
mature fruits.
We considered only the fleshy-fruited species in the
comparisons among the three sites, due to the predomi-
nance of animal dispersed fruits (mainly in intermediary
and foothill sites where they compose more than 90% of
individuals) and to eliminate the effect of the seed dispersal
syndrome in our results. Nonetheless, because 30% of
individuals are dry-fruited species in the seashore, we
presented the phenological patterns per seed dispersal mode
for this site.
We applied a circular statistic (Zar 1996) to detect
seasonal trends and compare phenological patterns among
sites. The circular statistic is a technique widely used in
phenological studies (for a complete review see Morellato
et al. 2010). The year was represented as a circle of 360˚
with an arbitrary origin (by convention, January corre-
sponds to 15˚). We estimated the peak date of all
phenophases for each individual observed, and we calcu-
lated the mean peak date (or mean angle), the length of the
vector r (the concentration around the mean angle) and the
circular standard deviation of the mean peak date (Zar
1996) for each site. To test for seasonality in the
reproductive patterns at each site, we tested for the
significance of the mean angles by applying the circular
Rayleigh test, Z as described in Morellato et al. (2000). If
the mean date or angle was significant, then the phenolog-
ical pattern was seasonal and the concentration around the
mean angle, denoted by r, was considered as a measure of
the degree of seasonality (Morellato et al. 2000). The vector
r varies from 0 (when angles or peak dates are uniformly
distributed throughout the year) to 1 (when angles or peak
dates are concentrated in one single mean date or mean
angle) (Zar 1996).
To test our prediction of increasing seasonality with
environmental variability, we used only the phenology of
the flesh fruit species in the second year of observations to
compare the sites for two main reasons. First, the peak
dates did not differ between the two years of study in the
intermediary or foothills for all phenological phases (Table
S2), except for flower buds in the intermediary, which
occurred only about 24 days laterin the second year.
Second, we detected differences between years in the
seashore (Table S2) due to the reproductive activity of
two supra-annual species, Erytroxyllum and Daphnopsis, in
846 Int J Biometeorol (2011) 55:843–854
the first year of study (Fig. S5); they generated a bimodal
distribution. If we remove the two supra-annuals, the
community pattern did not differ between years. Therefore,
we used only the phenology of the second year to compare
sites.
At a fine scale, we compared the mean peak date or
angle of each phenophase among sites, taking into account
the results of the Rayleigh test and applying the Watson-
Williams F test to check if the significant mean dates
differed (see Morellato et al. 2010, 2000 for details).
Because the assumptions of normality, homogeneity and
linearity were not met for all phenophases, we conducted
Spearman’s correlations to examine the association between
climatic factors (rainfall, temperature and day-length) and
phenological responses (% of individuals in activity in each
month). We used the Bonferroni correction to correct the
degrees of freedom.
Finally, to disentangle which factor—species composi-
tion or microenvironment—explains the differences in
phenology across sites, we controlled for species composi-
tion by examining the phenology of the two most abundant
species: Euterpe edulis and Ternstroemia brasiliensis. Thus,
we applied circular statistics, as previously described, to
test if the species mean angles or dates of reproductive
activity differed between vegetations through the Watson-
Williams test. If the mean angles of the species differed
between sites, we would consider that the phenological
variation among vegetations was related to microenviron-
mental factors. On the other hand, if the species mean angle
did not differ between sites we would consider the
phenological differences among vegetations would be better
explained by the species turnover along the sites.
Results
Microenvironment: characterization and comparison
among sites
Microenvironmental conditions differed between seasons
and among sites (Figs. 2 and 3). The canopy openness was
higher in the seashore (70 and 64% in the wet and less wet
seasons, respectively) due to the predominance of shrubs
and grasses (Fig. 2, Table S3). For the other sites, the
canopy openness was less than 10% (Fig. 2, Table S3).
Consequently, the PAR reaching the seashore was always
higher (up to 1000 μmol-1 m-2) than in the other sites. The
seashore also had the lowest relative humidity in both
seasons (64% and 53% in the wet and less wet seasons,
respectively; Fig. 2, Table S3). The relative humidity was
between 80% and 90% in the other two sites, except in the
dry season when the intermediary was drier than the
foothills (72% and 91% relative humidity, respectively). In
the wet season, temperatures were similar and around 25°C
(Fig. 2, Table S3), whereas the seashore was the warmest
site (22°C) followed by intermediary (19°C) and foothills
(17°C) during the less wet season.
As a consequence, the transects differed in microenvi-
ronment conditions, and the first ordination axis explained
74% of the existing microenvironmental variation (P<
0.001). It was mainly associated with light incidence,
separating the sampling into three groups that perfectly
matched with our a priori classification (seashore, interme-
diary and foothills; Fig. 3). Additionally, this axis was
negatively associated with PAR (eigenvector: −0.97),
canopy openness (−0.92) and temperature (−0.64) and
positively associated with relative humidity (eigenvector:
0.87) (Fig. 3). Moreover, the axis 2 was associated with
temperature (eigenvector: 0.76, Fig. 3), but it was not
significant. The sites were more similar in the wet season,
noted by the lower dispersion of the scores along axis 1,
than in the less wet season (Fig. 3).
Floristic comparisons
We sampled a total of 1,027 individuals distributed in 41
families and 106 plant species (Table S1). The most diverse
and abundant family at PEIC was Myrtaceae with 25
species and 204 individuals. Myrtaceae was also the most
diverse family in all three sites (5 species in the seashore,
15 in the intermediary and 10 in the foothills), although its
abundance ranking shifted among sites.
Myrtaceae was the most abundant in seashore vegetation
(19% of individuals), followed by Sapindaceae, represented
by the wind dispersed Dodonea viscosa (15%). Arecaceae,
with 28% of individuals (48% Geonoma schottiana and
44% Euterpe edulis), preceded Myrtaceae (19%) as the
most abundant family in intermediary vegetation. In
addition, Rubiaceae was the most abundant family
(29%) in the foothills, represented mainly by Psychotria
nuda, followed by Myrtaceae (22% of individuals),
represented mainly by Eugenia cuprea and Marlierea
tomentosa (Table S1).
Considering just the floristic composition, the seashore
and intermediary vegetations were more similar (12 co-
occurring species; Table 1). However, when we take into
account abundance, the intermediary and foothill vegeta-
tions were more similar, regardless the index (Table 1). The
differences among sites are illustrated in the DCA ordina-
tion of transects which incorporated both abundance and
species composition (Fig. 4).
Additionally, we found that habitats with a more
divergent microenvironment showed a more distinctive
abundance and composition of species. In other words,
the microenvironmental variables directly influence the
floristic-structural dissimilarities among the localities (stan-
Int J Biometeorol (2011) 55:843–854 847
dardized mantel statistic, r = 0.75; P=0.001; Zobs=532.90;
Zave=475.5). This means that when the microenvironmental
distance between localities is greater, their floristic-
structural differences are greater.
Phenology and seasonality
Over the 24 month of study, 74% of individuals reproduced
in at least one month. The seashore and intermediary
vegetations presented flower buds and flowers concentrated
at the beginning of the wet season and positively correlated
with increasing day-length (Fig. 5; Table 2). Conversely, in
the foothill vegetation, these phenophases presented a
bimodal pattern with a major peak in November to
December and a minor one from March to May (Fig. 5)
and no correlation with climatic factors (Table 2). On a large
scale, the phenological patterns observed for the vegetation
at the seashore, intermediary and foothill sites reinforced the
general patterns depicted in Fig. 1 (percent of species), with
a general increasing of phenological activity during the wet
Fig. 2 Box plots for the microenvironmental variables: temperature,
relative humidity, PAR (photosynthetically active radiation) and
canopy openness for the three sites in the Atlantic rainforest at
Cardoso Island, Southeastern Brazil. S seashore, I intermediary, F
foothills; Q1: lower quartile (25%), Q2: median, Q3: upper quartile
(75%)
848 Int J Biometeorol (2011) 55:843–854
and warm season for flowering and during the transition of
the seasons (wet–less wet) for fruiting (Fig. 5).
However, on a fine scale, considering the peak date of
each flesh fruited animal-dispersed plant per site, we
detected significant differences in the peak of phenological
activity among vegetations (Fig. 6; Table 3). The circular
analyses demonstrated that reproduction was significantly
seasonal in the three vegetations (Fig. 6), yet the mean peak
dates were significantly different between the three sites for
all phenophases except mature fruits (Fig. 6; Table 3). The
mature fruit mean peak date did not differ between
intermediary (11 March) and foothill (24 March) vegeta-
tions. Seasonality was higher for flower buds and flowers;
the highest values of concentration, vector r, ranged from
0.71 to 0.78 (Fig. 6). The foothills vegetation presented the
higher degree of seasonality (mean r among all pheno-
phases: 0.71) while the intermediary vegetation showed the
lowest degree of seasonality (mean r = 0.61; Fig. 6). The
difference could be relatedto the higher r values of fruiting
observed for the foothills vegetation, which was 8–35%
more concentrated compared to the other two vegetations
(see vectors r, Fig. 6).
The first flowering peak was observed in the foothills
vegetation (October 25 and November 5 for flower bud and
flower, respectively), followed by intermediary (November
25 and 30) and finishing at the seashore vegetation
(December 7 and 24) (Fig. 6). The same sequence was
observed for fruiting, the last peak occurring on April 23 at
the seashore vegetation (Fig. 6).
The dry-fruit species, which represent a significant part of
the scrub vegetation, presented two peaks of activity during
the year (Fig. 5), and fruiting was not seasonal (Fig. S6).
The two most abundant species (Euterpe edulis and
Ternstroemia brasiliensis) did not show consistent signifi-
cant differences in the mean peak angle between vegeta-
tions (Table S4).
Discussion
Coastal plain floristic and phenological diversity
The floristic diversity of the Atlantic rainforest is well
established (Caiafa and Martins 2010; Oliveira-Filho and
Fontes 2000; Scudeller et al. 2001), with great heterogene-
ity in the distribution and abundance of tree species.
Additionally, the coastal plain or restinga is regarded as a
vegetation complex (Scarano 2002), and recent studies have
confirmed the high variability of coastal plain lowland
vegetation across their large latitudinal range of distribution
over the Brazilian coast (see Marques et al. 2011 and
references therein). We confirmed the high diversity within
our study area with the remarkable floristic and phenolog-
ical differences among the three contiguous vegetations.
Fig. 3 Microenvironmental ordination using the principal component
analysis (PCA) technique. Symbols represent transects sampled in the
less wet (open symbols) and wet seasons (closed symbols) in the
Atlantic rainforest at Cardoso Island, Southeastern Brazil: seashore
(circles), intermediary (triangles) and foothills (diamonds)
Comparisons (number of co-occurring species) Qualitative indices Quantitative indices
Jaccard Sorensen Sorensen Morisita-Horn
Seashore and intermediary (12) 0.18 0.30 0.12 0.10
Seashore and foothills (4) 0.05 0.10 0.01 0.004
Foothills and intermediary (9) 0.10 0.19 0.15 0.20
Table 1 Comparisons of the
Atlantic rainforest vegetation
types at Cardoso Island using
qualitative (comparing species
composition) and quantitative
(comparing species composition
and abundance) indices
Int J Biometeorol (2011) 55:843–854 849
We consider the seashore the more extreme environment
for plants due to the highest range of microenvironmental
values observed within and between seasons. The lowest
canopy cover and highest PAR values characterize a higher
light incidence than in the other vegetations studied (Fig. 2;
Table S3). As a result, the relative humidity was lower and
temperatures were higher in the seashore. Our conclusion is
in agreement with the overall literature describing the
seashore as an extreme environment, exposing the vegeta-
tion to more severe conditions for growth and reproduction
(Seeliger 1992; Scarano 2002). Therefore, we consider the
divergent microenvironmental conditions as the main
environmental filter driving the differences among vegeta-
tions types, as proposed by Bernardi et al. (2005) and
Gentry and Emmons (1987). Differences in temperature and
humidity are regarded as the key factors defining species
occurrence at a local scale (Oliveira-Filho and Fontes 2000;
Pyke et al. 2001). The differences in microenvironment
determined the species composition, which, as a conse-
quence, shaped the reproductive phenology of the vegeta-
tions studied.
Coarse and fine scale comparisons among the sites
On a coarse scale, considering just the proportion of species
or plants reproducing, the three sites presented some degree
of seasonality since all increased the offer of flowers in the
wet season and fruits in the transition wet–less wet season.
A similar pattern is described for other Atlantic rainforests
from Southeastern and Southern Brazil (Marques and Oliveira
2004; Marques et al. 2004; Morellato et al. 2000; Talora and
Morellato 2000). Day-length and temperature remain as the
main abiotic factors influencing Atlantic rainforest phenology
(see Morellato et al. 2000). The more extreme microenvir-
onmental conditions of the open, dryer vegetation of the
seashore did not constrain flowering or fruiting to a specific
time of the year when compared to the other two forest sites
studied. This finding suggests that the species are well
adapted to those stressful conditions (Scarano 2002; Seeliger
1992). Reproductive activity during the year, regardless of
the degree of vegetation seasonality, has been observed for
other restinga vegetations in the Atlantic rainforest (Marques
and Oliveira 2004; Talora and Morellato 2000).
On a fine scale, when taking into account the peak of
phenological activity, the significant differences observed
Fig. 5 Percent of individuals flowering (upper bars) and fruiting
(lower bars) in the three vegetations studied on the seashore,
intermediary and foothill sites of the Atlantic rainforest at Cardoso
Island, Southeastern Brazil
Fig. 4 Ordination (DCA) of seashore (circles), intermediary (triangles)
and foothill (diamonds) vegetations in accordance with the abundance
and composition of species in the Atlantic rainforest at Cardoso Island,
Southeastern Brazil. Symbols represent transects sampled and dots
represent the species
850 Int J Biometeorol (2011) 55:843–854
among the three vegetations matched the differences in
floristic composition, revealing a local temporal diversity.
We considered that the species turnover along the sites is
the most important factor driving the phenological differ-
ences among the vegetations studied because the mean peak
angle did not show consistent differences for the two most
abundant species (Euterpe edulis and Ternstroemia brasi-
liensis). We found that three out of fourteen cases showed
significant differences. Bencke and Morellato (2002)
reported phenological differences for two out of nine
species compared across three Atlantic rainforest vegeta-
tions, including two restinga forests. A previous study at
Cardoso Island (intermediary and foothills) reported seven
significant differences out of twelve comparisons in the
reproductive phenology of Euterpe edulis (Castro et al.
2007), although they compared the frequency of reproduc-
tive individuals per month instead of mean peak angles.
The local differences of fruiting time may be related to
the temporal variation of certain microenvironmental con-
ditions in each of the vegetation studied. For instance, the
warmest less wet season in the seashore compared to the
higher humidity and lower temperatures in the intermediary
and foothill sites. The lower temperatures are suggested to
favor fruiting of animal-dispersed Atlantic rainforest trees
(Morellato et al. 2000).
If we consider the peak date of flowering or fruiting of
each individual as a proxy for resource availability, the
divergent distribution of mean peak dates of flowering and
fruiting at each site uncoupled the sites’ phenology along
the main reproductive season (Fig. 6). The availability of
food resources is of upmost importance in tropical forests,
where the majority of plant species rely upon animal
vectors for pollination and seed dispersal (Jordano 1995;
Memmott et al. 2007). Therefore, fine phenological
divergences at a local scale provide a mosaic of food
resources that has consequences for the maintenance of
animals (see Haugaasen and Peres 2005), such as frugi-
vores and flower visitors.
Concluding remarks
Our study reveals that the spatial diversity observed in the
structure and composition of the tropical forests studied was
the main factor determining each vegetation phenology, which
we define as phenological diversity. The phenological
diversity has been observed when taking into account the
plants’ phenological strategies(e.g., Bawa et al. 2003;
Newstrom et al. 1994), but just occasionally is it analyzed
from the spatial point of view of the heterogeneity within
vegetation types (Heideman 1989; Bencke and Morellato
2002; Castro et al. 2007) or even within species and
individuals (Goulart et al. 2005; Bendix et al. 2006). We
observed an exchange of species providing flowers and fruits
across the coastal plain vegetation complex represented by
the seashore, intermediary and foothill vegetations.
We conclude that the general phenological patterns, as
described in many tropical phenology papers, may conceal
the fine scale temporal phenological diversity. Our study
indicates that microenvironmental heterogeneity influences
floristic diversity and generates temporal or phenological
Location Vegetation type Day-length Mean temperature Rainfall
Seashore Flower bud 0.86 ** 0.33 −0.09
Flower 0.80 ** 0.42 −0.07
Immature fruit 0.34 0.76 ** 0.38
Mature fruit −0.35 0.14 0.58*
Intermediary Flower bud 0.83 ** 0.46 0.04
Flower 0.64 ** 0.23 −0.04
Immature fruit 0.83 ** 0.71** 0.14
Mature fruit −0.15 0.35 0.66**
Foothills Flower bud 0.46 0.41 0.01
Flower 0.16 0.26 0.05
Immature fruit 0.78 ** 0.68** 0.21
Mature fruit 0.03 0.55 0.46
Table 2 Spearman rank correla-
tion tests between the percent-
age of individuals on each
phenophase and environmental
factors during 24 months of
study, for each vegetation type
in the Atlantic rainforest at
Cardoso Island, Southeastern
Brazil
Bonferroni correction was
applied (significant results:
P≤0.004). **P≤0.001;
*P≤0.003
Table 3 Comparisons of the mean reproductive peak date (Watson-
Williams F test) among vegetation types for all phenophases in the
Atlantic rainforest at Cardoso Island, Southeastern Brazil
Sites Flower bud Flower Immature fruit Mature fruit
F X S 41.05 *** 50.94 *** 32.91 *** 8.91 **
F X I 12.74 ** 9.03 ** 8.03 ** 1.09 NS
S X I 4.23 * 14.91 *** 6.06 * 12.86 ***
F foothills, S seashore, I intermediary
Significance: *P≤0.05, **P≤0.001, **P≤0.0001
Int J Biometeorol (2011) 55:843–854 851
852 Int J Biometeorol (2011) 55:843–854
diversity, which certainly contributes to the overall Atlantic
rainforest diversity of species. Finally, the integration of
local, historical and sensor-derived phenologies has brought
phenology to a global scale (Liang and Schwartz 2009;
Rutishauser et al. unpublished data). However, when
downscaling sensor-derived phenology or “pixel phenology”
derived from instrument-base observation to ground “species
phenology” (Rutishauser et al. unpublished data), one should
carefully consider the phenological diversity on a local scale,
especially within the highly diverse tropical forests.
Acknowledgments We are grateful to the Instituto Florestal for
allowing our research at the Ilha do Cardoso State Park, to FAPESP
(Fundação de Amparo à Pesquisa do Estado de São Paulo) for the
financial support (n˚06/61759-0 and 08/08344-2) and the master
scholarship to V.G.S. (n˚ 05/57739-1) and to Cláudio Bernardo for
assistance in the field. L.P.C.M. receives a research productivity
fellowship and grant from the CNPq (Conselho Nacional de
Desenvolvimento Científico e Tecnológico). We also thank M. Sobral
for the identification of Myrtaceae species and L.M. Bini for statistical
advice.
References
Barros F, Melo MMRF, Chiea SAC, Kirizawa M, Wanderley MGL,
Jung-Mendaçolli SL (1991) Flora fanerogâmica da Ilha do
Cardoso. Boletim do Instituto de Botânica 1:1–184
Bawa KS, Kang H, Grayum MH (2003) Relationships among time,
frequency, and duration of flowering in tropical rain forest trees.
Am J Bot 90(6):877–887. doi:10.3732/ajb.90.6.877
Bencke CSC, Morellato LPC (2002) Estudo comparativo da fenologia
de nove espécies arbóreas em três tipos de floresta atlântica no
sudeste do Brasil. Revista Brasileira de Botânica 25(2):237–248.
doi:10.1590/S0100-84042002000200012
Bendix J, Homeier J, Cueva Ortiz E, Emck P, Breckle S, Richter M,
Beck E (2006) Seasonality of weather and tree phenology in a
tropical evergreen mountain rain forest. Int J Biometeorol 50
(6):370–384. doi:10.1007/s00484-006-0029-8
Bernardi JVE, Landim PMB, Barreto CL, Monteiro RC (2005) Estudo
espacial do gradiente de vegetação do Parque Estadual da Ilha do
Cardoso, SP, Brasil. Holos Environ 5(1):1–22
Boulter SL, Kitching RL, Howlett BG (2006) Family, visitors and the
weather: patterns of flowering in tropical rain forests of northern
Australia. J Ecol 94(2):369–382. doi:10.1111/J.1365-
2745.2005.01084.X
Caiafa A, Martins F (2010) Forms of rarity of tree species in the
southern Brazilian Atlantic rainforest. Biodivers Conserv 19
(9):2597–2618. doi:10.1007/s10531-010-9861-6
Camargo M, Souza R, Reys P, Morellato L (2011) Effects of cardinal
orientation and light on the reproductive phenology of the
cerrado savanna tree Xylopia aromatica (Annonaceae). Anais da
Academia Brasileira de Ciências 83(3):1–13
Castro E, Galetti M, Morellato L (2007) Reproductive phenology of
Euterpe edulis (Arecaceae) along a gradient in the Atlantic
rainforest of Brazil. Aust J Bot 55:725–735. doi:10.1071/bt07029
Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S,
Gunatilleke N, Hubbell SP, Foster RB, Itoh A, LaFrankie JV, Lee
HS, Losos E,ManokaranN, Sukumar R, Yamakura T (2000) Spatial
patterns in the distribution of tropical tree species. Science 288
(5470):1414–1418. doi:10.1126/science.288.5470.1414
Couto OS, Cordeiro RMS (2005) Manual de reconhecimento das
espécies vegetais da restinga do Estado de São Paulo. Secretaria
do Meio Ambiente, Departamento Estadual de Proteção aos
Recursos Naturais – DEPRN – São Paulo: SMA 2005, São Paulo
Fournier LA (1974) Un método cuantitativo para la medición de
características fenológicas en árboles. Turrialba 24(4):422–423
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(3):881–919
Frazer G, Canham C, Lertxman K (1999) Gap Light Analyzer (GLA)
version 2.0: imaging software to extract canopy structure and gap
light transmission indices from true-colour fisheye photographs,
users manual and program documentation. Simon Fraser Univer-
sity, Burnaby, British Columbia, Canada and the Institute of
Ecosystem Studies, Millbrook, New York, USA
Gentry AH (1988) Changes in plant community diversity and floristic
composition on environmental and geographical gradients. Ann
Missouri Bot Gard 75(1):1–34
Gentry AH, Emmons LH (1987) Geographical variation in fertility,
phenology, and composition of the understory of neotropical
forests. Biotropica 19(3):216–227
Goulart MF, Lemos JP, Lovato MB (2005) Phenological variation
within and among populations of Plathymenia reticulata in
Brazilian Cerrado, the Atlantic forest and transitional sites. Ann
Bot 96(3):445–455. doi:10.1093/aob/mci193
Haugaasen T, Peres CA (2005) Tree phenology in adjacent Amazonian
flooded and unflooded forests. Biotropica 37(4):620–630.
doi:10.1111/j.1744-7429.2005.00079.x
Heideman PD (1989) Temporal and spatial variation in the phenology
of flowering and fruiting in a tropical rainforest. J Ecol 77
(4):1059–1079
Hubbell SP (1979) Tree dispersion, abundance, and diversity in a
tropical dry forest. Science 203(4387):1299–1309. doi:10.1126/
science.203.4387.1299
Janzen DH (1967) Synchronization of sexual reproduction of trees
within the dry season in Central America. Evolution 21(3):620–
637
Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a
comparative analysis of adaptation and constraints in plant-
animal interactions. Am Nat 145(2):163–191
Köppen W (1923) Die Klimate der Erde. Walter de Gruyter, Berlin
Legendre P, Legendre L (1998) Numerical ecology. Elsevier,
Amsterdam
Liang L, Schwartz M (2009) Landscape phenology: an integrative
approach to seasonal vegetation dynamics. Landsc Ecol 24
(4):465–472. doi:10.1007/s10980-009-9328-x
Manly BFJ (2004) Multivariate statistical methods: a primer, 3rd edn.
Chapman & Hall/CRC, USA
Marques M, Oliveira P (2004) Fenologia de espécies do dossele do
sub-bosque de duas Florestas de Restinga na Ilha do Mel, sul do
Brasil. Revista Brasileira de Botânica 27:713–723. doi:10.1590/
S0100-84042004000400011
Marques MCM, Roper JJ, Salvalaggio APB (2004) Phenological
patterns among plant life-forms in a subtropical forest in southern
Braz i l . P l an t Eco l 173(2 ) :203–213 . do i :10 .1023 /
B:VEGE.0000029325.85031.90
Fig. 6 Frequency distribution of individual peak dates of flower bud
(a), flower (b), immature fruit (c) and mature fruit (d) for fleshy-
fruited species from September 2008 to August 2009 (year 2) in the
three vegetations studied on the seashore, intermediary and foothill
sites of the Atlantic rainforest at Cardoso Island, Southeastern Brazil.
All mean angles (ā±1 SD) are significant (Rayleigh test, P<0.001)
and the arrows point to the mean direction. Vector r (0 to 1) indicates
the concentration around the mean angle and N indicates the number
of observed individuals
R
Int J Biometeorol (2011) 55:843–854 853
http://dx.doi.org/10.3732/ajb.90.6.877
http://dx.doi.org/10.1590/S0100-84042002000200012
http://dx.doi.org/10.1007/s00484-006-0029-8
http://dx.doi.org/10.1111/J.1365-2745.2005.01084.X
http://dx.doi.org/10.1111/J.1365-2745.2005.01084.X
http://dx.doi.org/10.1007/s10531-010-9861-6
http://dx.doi.org/10.1071/bt07029
http://dx.doi.org/10.1126/science.288.5470.1414
http://dx.doi.org/10.1093/aob/mci193
http://dx.doi.org/10.1111/j.1744-7429.2005.00079.x
http://dx.doi.org/10.1126/science.203.4387.1299
http://dx.doi.org/10.1126/science.203.4387.1299
http://dx.doi.org/10.1007/s10980-009-9328-x
http://dx.doi.org/10.1590/S0100-84042004000400011
http://dx.doi.org/10.1590/S0100-84042004000400011
http://dx.doi.org/10.1023/B:VEGE.0000029325.85031.90
http://dx.doi.org/10.1023/B:VEGE.0000029325.85031.90
Marques M, Swaine M, Liebsch D (2011) Diversity distribution and
floristic differentiation of the coastal lowland vegetation: implica-
tions for the conservation of the Brazilian Atlantic Forest. Biodivers
Conserv 20(1):153–168. doi:10.1007/s10531-010-9952-4
Melo MMRF, Mantovani W (1994) Composição florística e estrutura do
trecho de mata atlântica de encosta, na Ilha do Cardoso (Cananéia,
SP, Brazil). Boletim do Instituto de Botânica 9:107–157
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming
and the disruption of plant–pollinator interactions. Ecol Lett 10
(8):710–717. doi:10.1111/j.1461-0248.2007.01061.x
Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC,
Zipparro VB (2000) Phenology of Atlantic rain forest trees: a
comparative study. Biotropica 32(4b):811–823. doi:10.1111/
j.1744-7429.2000.tb00620.x
Morellato LPC, Alberti LF, Hudson IL (2010) Applications of circular
statistics in plant phenology: a case studies approach. In: Hudson
IL, Keatley MR (eds) Phenological research. Springer, Nether-
lands, pp 339–359. doi:10.1007/978-90-481-3335-2_16
Newstrom LE, Frankie GW, Baker HG (1994) A new classification for
plant phenology based on flowering patterns in lowland tropical
rain-forest trees at La-Selva, Costa-Rica. Biotropica 26(2):141–159
Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differen-
tiation among Atlantic forests in southeastern Brazil and the
influence of climate. Biotropica 32(4b):793–810. doi:10.1646/
0006-3606(2000)032[0793:POFDAA]2.0.CO;2
Pereira AR, Angelocci LR, Sentelhas PC (2001) Agrometeorologia:
fundamentos e aplicações práticas. Editora Agropecuária, Guaíba
Pinto MM (1998) Fitossociologia e influência de fatores edáficos na
estrutura da vegetação em áreas de Mata Atlântica na Ilha do
Cardoso - Cananéia, SP. PhD thesis, UNESP, Jaboticabal, Brasil
Pyke CR, Condit R, Aguilar S, Lao S (2001) Floristic composition
across a climatic gradient in a neotropical lowland forest. J Veg
Sci 12(4):553–566. doi:10.2307/3237007
Richards PW (1996) The tropical rain forest, 2nd edn. Cambridge
University Press, Cambridge. doi:10.2277/0521421942
Sakai S (2001) Phenological diversity in tropical forests. Popul Ecol
43(1):77–86. doi:10.1007/PL00012018
Scarano FR (2002) Structure, function and floristic relationships of
plant communities in stressful habitats marginal to the Brazilian
Atlantic rainforest. Ann Bot 90(4):517–524. doi:10.1093/aob/
mcf189
Schwartz MD, Hanes JM (2010) Intercomparing multiple measures of
the onset of spring in eastern North America. Int J Climatol 30
(11):1614–1626. doi:10.1002/joc.2008
Scudeller V, Martins F, Shepherd G (2001) Distribution and abundance
of arboreal species in the Atlantic ombrophilous dense forest in
Southeastern Brazil. Plant Ecol 152(2):185–199. doi:10.1023/
a:1011494228661
Seeliger U (1992) Coastal plant communities of Latin America.
Academic Press Inc., London
Sugiyama M (1998) Estudo de florestas de restinga da Ilha do
Cardoso, Cananéia, São Paulo, Brasil. Boletim do Instituto de
Botânica 11:119–159
Talora DC, Morellato LPC (2000) Fenologia de espécies arbóreas em
floresta de planície litorânea do sudeste do Brasil. Revista
Brasileira de Botânica 23(1):13–26. doi:10.1590/S0100-
84042000000100002
van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of
tropical forests: adaptive significance and consequences for
primary consumers. Ann Rev Ecol Syst 24:353–377.
doi:10.1146/annurev.es.24.110193.002033
Wheelwright NT (1985) Competition for dispersers, and the timing of
flowering and fruiting in a guild of tropical trees. Oikos 44
(3):465–477
Zar JH (1996) Biostatiscal analysis. Prentice-Hall International,
London
854 Int J Biometeorol (2011) 55:843–854
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http://dx.doi.org/10.1646/0006-3606(2000)032<0793:POFDAA>2.0.CO;2
http://dx.doi.org/10.1646/0006-3606(2000)032<0793:POFDAA>2.0.CO;2
http://dx.doi.org/10.2307/3237007
http://dx.doi.org/10.2277/0521421942
http://dx.doi.org/10.1007/PL00012018
http://dx.doi.org/10.1093/aob/mcf189
http://dx.doi.org/10.1093/aob/mcf189
http://dx.doi.org/10.1002/joc.2008
http://dx.doi.org/10.1023/a:1011494228661
http://dx.doi.org/10.1023/a:1011494228661
http://dx.doi.org/10.1590/S0100-84042000000100002
http://dx.doi.org/10.1590/S0100-84042000000100002
http://dx.doi.org/10.1146/annurev.es.24.110193.002033
https://www.researchgate.net/publication/51556836
	Reproductive phenology of coastal plain Atlantic forest vegetation: comparisons from seashore to foothills
	Abstract
	Introduction
	Materials and methods
	Study area
	Plant survey and microenvironmental variables
	Floristic comparisons
	Phenological sampling and data analyses
	Results
	Microenvironment: characterization and comparison among sites
	Floristic comparisons
	Phenology and seasonality
	Discussion
	Coastal plain floristic and phenological diversity
	Coarse and fine scale comparisons among the sites
	Concluding remarks
	References