Journal of

Ecology

2006

94

, 369382

2006 The Authors
Journal compilation
2006 British
Ecological Society

Blackwell Publishing Ltd

Family, visitors and the weather: patterns of owering in
tropical rain forests of northern Australia

S.L. BOULTER, R.L. KITCHING and B.G. HOWLETT*

Cooperative Research Centre for Tropical Rainforest Ecology and Management, Australian School of Environmental
Studies, Grifth University, Nathan, Queensland 4111, Australia

Summary
1

A data base on the owering phenology of the Wet Tropics bioregion of far northern
Queensland, Australia, has been constructed, based upon over 36 774 records from two
Queensland-based herbaria.

2

Flowering patterns have been analysed against the predictions of three overlapping
hypotheses based on climatic, biotic and phylogenetic explanations. No one hypothesis
is supported to the exclusion of the others.

3

Patterns of owering in the Wet Tropics show marked seasonal increases and
decreases, except in the northern lowlands. In general this seasonality correlates with
rainfall and temperature and is exacerbated by increasing latitude and altitude.

4

There is little or no statistical evidence for the over-dispersion of owering times that
would indicate a competition-avoidance mechanism: owering within taxa or morpho-
logical groups tends to be clumped (and if not, is random).

5

That clumping of owering within taxa does not coincide with a single season
provides support for a mass action hypothesis based on the minimization of generalist
predation and/or the avoidance of ower predation.

6

Timing of owering did show some consistency among species within genera
and within families, but there was little consistency at higher taxonomic levels. Clear
separation of the biotic and phylogenetic hypotheses requires greater knowledge of
pollination ecology and phylogeny of this large and diverse ora.

7

Understanding of owering patterns and their underlying determining mechanisms
is a key to assessing the ecosystem health of the forest. Our results highlight the importance
of competitive interactions and of physical and evolutionary factors as determinants
of owering time, intensity and co-occurrence in tropical forests.

Key-words

: climate, owering phenology, herbaria, phylogeny, rainfall, rain forest,
seasonality, synchronous owering

Journal of Ecology

(2006)

94

, 369382
doi: 10.1111/j.1365-2745.2005.01084.x

Introduction

Understanding owering phenology in tropical rain
forests presents problems not encountered in better-
known temperate oras. Three characteristics represent
particular challenges to the tropical ecologist: geo-
graphical position, biological richness and availability
of information. The low latitudes, mesic climates and
associated year-round biological activity characteristic
of many tropical forests means that the mere proposition
of seasonality in any phenological feature, including
owering, needs to be established rather than assumed.
Secondly, most tropical rain forests exhibit levels of
plant species richness an order of magnitude greater
than those encountered in temperate regions. This rich-
ness includes substantial co-occurrence of congeners
and con-familials. Coupled with a high diversity of
potential animal pollinators this raises interesting and
challenging hypotheses related to resource-partitioning
within and among plant taxa. Lastly, there are rela-
tively few tropical rain forest oras for which we have
sufcient information to be able to make statistically
valid tests of hypotheses at the level of the entire ora.

Correspondence: S. L. Boulter (fax + 61 73875 55014; e-mail
s.boulter@grifth.edu.au).
*Present address: New Zealand Institute for Crop and Food
Research Ltd, Private Bag 4074, Christchurch, New Zealand.
370

S. L. Boulter,
R. L. Kitching &
B. G. Howlett

2006 The Authors
Journal compilation
2006 British
Ecological Society,

Journal of Ecology

94

, 369382

Flowering is the precursor to the reproductive events
that determine the future sustainability of the species.
Timing, duration and frequency of owering are all
known to vary amongst individual species in tro-
pical forests (Bawa

et al

. 2003; Borchert

et al

. 2004).
Deciphering the proximate cues and ultimate causes
of phenological variation has led, on one hand, to an
expectation that phenological patterns are adaptive,
leading to the synchronization of reproductive activity
with the availability of biotic resources (i.e. pollinators,
predators) and with the peak availability of abiotic
resources (e.g. sunlight, water). Alternate theories are
based on evidence that phenological patterns are not
adaptive, and are therefore conserved among closely
related taxa. Numerous hypotheses have been formulated
regarding the inuence of various factors on owering
phenology (see reviews in Wright & van Schaik 1994;
Bawa

et al

. 2003; Bolmgren

et al

. 2003) and fall into
three categories, as summarized below.

Climatic hypotheses

, of which several have been
developed, link seasonal increases of phenological
activity to predictable seasonal variation in limiting
factors. These include the presence of seasonally vari-
able pollinators (Waser 1979; Rathcke & Lacey 1985)
and predators (Wright & van Schaik 1994), conditions
favourable to dispersal or germination (Frankie

et al

.
1974; Heideman 1989; Ramrez 2002) and variation in
environmental factors that favour or limit plant pro-
duction, and therefore reproduction (Borchert 1983;
van Schaik

et al

. 1993; Wright & van Schaik 1994). The
relative importance of these inuences will vary among
sites. For example, where forests are dry, moisture avail-
ability is expected to become important (Wright &
Cornejo 1990), whereas where water is not limited
other aspects of seasonality (e.g. solar irradiance,
Wright & van Schaik 1994; Graham

et al

. 2003) may be
of greater importance. The phenology of individual
species can also be a factor of a trees functional type
(Borchert

et al

. 2004).

Biotic hypotheses

link the activities of pollinator,
predator and dispersers to the synchrony of owering
in individual plants (Wright 1996). One such, the

pol-
linator competition hypothesis

, assumes that pollinators
are a limiting resource and owering events should be
evenly spread through time, a staggered phenological
community (Pleasants 1980; Bolmgren

et al

. 2003).
This should be more especially the case for species
within genera or genera within families where a
common origin and morphology may be expected to
demand a common suite of pollinators (Pleasants
1980; Primack 1985). The main alternative hypothesis,

mass action

, suggests that facilitation will be more
important than competition and predicts that tem-
poral clumping of owering periods will both increase the
likelihood of successful pollination and decrease the
risk of predation upon individual owers by spreading
the risk across more individuals (Rathcke 1983; Sakai
2002). As the hypothesis is based on pollination inter-
actions being less specialized, it is assumed that the risk
of receiving foreign pollen is less than the benets of
increased visitation (failure of this assumption, of
course, might lead to selection for increased synchrony
within species and decreased synchrony among species).
The

phylogenetic hypothesis

proposes that owering
patterns are in some way inuenced or constrained by
phylogeny and as a result, taxonomically related species
will tend to show similar owering times (Waser 1979;
Kochmer & Handel 1986; Johnson 1992; Bolmgren

et al

. 2003; but see Ollerton & Lack 1992). Similarities
in related groups may include owering duration and
intensity (Johnson 1992). Kochmer & Handel (1986)
showed, for example, that certain angiosperm families
owered at particular times of the year between con-
tinents. Again, this hypothesis relaxes the supposition of
pollinators as a limiting resource and may imply, in
consequence, less specialized co-evolutionary interac-
tions between the trees and their associated pollinators.
We make three further points regarding studies of
owering phenology. First, the predicted outcomes of
the putatively separate hypotheses, such as temporal
clumping of owering activity, may, in fact, be indis-
tinguishable (Rathcke & Lacey 1985). Secondly, care
is needed to distinguish between the ultimate cause
of phenological patterns and the proximate cues that
individual plants respond to. Theoretical explanations
of phenological diversity generally address ultimate
causes. For example, in certain tree species, environ-
mental change is known to trigger the phenological
events that precede owering. In this case, climatic cues
are proximate mechanisms although these may also
have been selected for in response to environmental
or biotic adaptive pressures (Borchert

et al

. 2004).
Thirdly, the operation of all the various hypotheses
may operate, or be detected, at a variety of levels, from
microsite to landscape or community level (Borchert

et al

. 2004). The resulting phenological community
pattern is likely, by default, to partially represent vari-
ation at smaller scales (see, for example, discussions in
Bolmgren

et al

. 2003; Borchert

et al

. 2004).
We examine the community-wide patterns of ower-
ing phenology within the tree ora of the wet tropical
rain forests of far northern Queensland, Australia
(referred to as the Wet Tropics bioregion) using her-
barium records. We examine the resultant data base
for evidence of the main predictions of the alternate
hypotheses concerning the evolution and co-evolution
of owering patterns.
We ask the following:

1.

Does owering activity coincide with seasonal vari-
ation in climate at the level of the entire community
and, in consequence, are owering patterns accentuated
with increased latitude and altitude (Burger 1974; Borchert

et al

. 2004)?

2.

Is there evidence of the coincidence (clumping) or
divergence (staggering) of owering among species
that would be expected to share pollinators?

3.

Is there evidence that relatedness affects the timing,
concentration and duration of owering?
371

Rain forest
owering in
northern Australia

2006 The Authors
Journal compilation
2006 British
Ecological Society,

Journal of Ecology

94

, 369382

Methods

1nr rci oN

The Wet Tropics bioregion (15

39

to 19

17

S, 144

58

to 146

27

E) lies along the tropical north-east coast of
Queensland, from Black Mountain in the north to
approximately Townsville in the south. It is recognized
for its high oristic diversity (Myers

et al

. 2000). The
1.8

x

ha bioregion is dominated by rain-forested
mountains with extensive plateau areas along its west-
ern margin and lowland coastal plains along the east-
ern margin (Sattler & Williams 1999). Approximately
3000 species of plants are recorded in the bioregion,
with more than 700 species (23%) endemic to the area
(Sattler & Williams 1999). The region has a consider-
able range of climates associated with gradients of alti-
tude and annual rainfall. Mean annual rainfall ranges
from more than 3000 mm to less than 1600 mm (Tracey
1982). The Wet Tropics can be classed as seasonally
dry, with at least 5 months of the year receiving less
than 60 mm average rainfall (van Schaik

et al

. 1993).
November is the rst month to receive greater than
60 mm on average at most sites, with a summer wet season
continuing into March.

n:1: n:sr coNs1ic1i oN

A data base has been constructed that collates data on
the owering phenology of individual species of trees
and shrubs recorded from rain forest of the Wet Tropics
bioregion. Records of the month, altitude and latitude
of collection of all specimens possessing reproductive
structures (owers or buds) were taken from herbarium
specimen sheets at the North Queensland herbarium.
Additional records of the same species from the same
region have been accessed through HERBRECS, the
collection data base of the Queensland Herbarium,
Brisbane. A total of over 112 000 records were exam-
ined, of which some 36 774 were owering specimens
when collected. All native tree and shrub species
from the far north Queensland Wet Tropics bioregion
described in Hyland

et al

. (1999) have been included.
Species from the families Asteraceae, Commelinaceae,
Ericaceae and Plumbaginaceae that were listed by
Hyland

et al

. (1999) as predominantly herbaceous
with occasional shrub forms were not included. All
species from the families Cyperaceae, Juncaceae, Lil-
iaceae, Orchidaceae, Poaceae and Zingiberaceae were
also excluded. The tree ora that we have investigated
comprises 1267 species. These include members of 118
families.
Individual owering records were subdivided into
biogeographical units based on latitude and altitude of
collection point. Records were deemed to be northern
if they were recorded at less than 17

south or south-
ern if they were collected at latitudes greater than 17

south. This division coincides with the Black Moun-
tain Corridor or Gap, an area that divided the Wet
Tropics rain forest into two discrete refugia during the
most recent glacial period (Nix & Switzer 1991). This
divide is believed to have inuenced the distribution
of vertebrates in the bioregion (Winter 1997; Schneider
& Moritz 1999). Records were also categorized by
altitude using a modication of the classication
described in Tracey (1982). Records of specimens
collected at

<

400 m were classied as lowland, at
400800 m as upland and at

>

800 m as highland.

ir-:N:ixsrs

To check for any bias in collection times that would
determine the patterns of owering seen in the records,
we collated the collection month of all specimens (both
sterile and reproductive) for all species selected, from
the two herbarium collections. The number of species
collected by month was markedly different from the
number of owering specimens collected (Fig. 1). The
total number of specimens (both owering and sterile)
collected in a month was randomly distributed across
the course of the year (Runs test

P



=

0.113).

:N:ixsrs

The analysis uses statistical techniques widely used in
other phenological studies (e.g. Wright & Calderon
1995; Davies & Ashton 1999; Hamann 2004). To esti-
mate the mean owering times or owering midpoint,
circular vector statistics were employed as owering
events for individual species frequently span the break
in years, making it inappropriate to use linear models
based on a simple numbering of months.
For all species with 10 or more records the owering
midpoint was calculated as the angle of the mean
vector,

=

arctan(

y/x

) if

x



>

0
or

=

180

+

arctan(

y/x

) if

x



<

0 eqn 1
where

n

i

is the number of ower records in month

i

and

i

is
the midpoint of month

i

expressed as an angle

.

The rst
of January was chosen as 0

, with the midpoint of January
expressed as 15

and the midpoint of each succeeding
month arbitrarily assigned at 30

increments from that
point.
We also calculated the length of the mean vector
length,

r

, as a measure of the concentration of ower-
ing times for all species for which owering midpoint
was calculated (Batschelet 1981):
eqn 2
x n y n
i i i i
cos , sin = =
r x y n
i
( ) / = +
2 2
1
2
372

S. L. Boulter,
R. L. Kitching &
B. G. Howlett

2006 The Authors
Journal compilation
2006 British
Ecological Society,

Journal of Ecology

94

, 369382

We tested the relationship between mean vector length
and sample size and found no correlation.
Distributions of owering times, peak owering and
number of species collected over time, were tested for
randomness using Runs tests (Sokal & Rohlf 1995).

cii x:1r nxio1nrsrs

Patterns of peak owering were examined collectively
across the ora using all species for which the owering
midpoint was determined, and these were compared
with climatic patterns for the region to determine
if owering peaks coincide with particular climatic
events. Records were then further divided into north-
ern and southern and the owering peak re-examined.
Finally, this was repeated after further dividing the
owering records among the three altitudinal categories.
Runs tests were used to determine if seasonal trends
were demonstrated (Sokal & Rohlf 1995).

ni o1i c nxio1nrsrs

To determine if there is evidence that owering of Wet
Tropics species was selected to avoid pollinator com-
petition or enhance pollinator visitation, the overlap of
species that probably share pollinators was quantied
and tested to determine if this differed from random
expectation. Pollination data were available for no
more than a dozen or so of the Wet Tropics owering
plants, and we therefore used information on closely
related species groups to assign species to groups that
are likely to share pollinators. The overlap of owering
times for selected species was calculated using a pair-
wise overlap model (Pleasants 1980, 1990; Wright &
Calderon 1995). For each species, the proportion of
owering recorded in each month was calculated. The
overlap between all pairs of species was calculated as:
eqn 3
where

p

ik

and

p

jk

are the proportion of owering records
for species

i

and

j

recorded in the

k

th month. The mean
temporal overlap value was calculated for all pairwise
combinations. To generate the null model, the month
of the start of owering was selected randomly for each
species in a taxonomic group (family or genus). The shape
of the owering curve for each species was retained in
these simulations. In the case of those groups of species
where owering did not occur year-round, the start date
was generated to ensure owering would not extend
beyond the owering season. The mean of all pairwise
combinations was then calculated. This procedure was
repeated 1000 times. The actual mean overlap index
was then compared with the mean of the simulated
values. If the actual mean was greater than the median
95 percentile (i.e. greater than 97.5% of the simulated
values, equivalent to a

P

-value of 0.05 in a two-tailed test)
of the simulated values, owering was seen as consis-
tent with an aggregated distribution. If the actual
mean fell below this 95 percentile (i.e. less than 97.5% of
simulated values), then owering was categorized as stag-
gered. This test was performed for the 20 families that
had at least eight species with eight or more owering
records (Table 1) and for all genera with at least ve
species with eight or more owering records (Table 2).
To determine if a sample-size effect would bias the out-
come of this test, the data set for all families was strat-
ied into those species with greater than eight records,
those with greater than 14 records and those with greater
than 20 records and the test re-run to see if a greater
sample size improved the chances of a signicant result.
Analysis of data subdivided by altitude and latitude
tested whether the over-dispersion hypothesis operates
locally rather than regionally, but concerns about
statistical power meant that this was only possible for the
Myrtaceae, Lauraceae, Sapindaceae and Euphorbiaceae.

inxiocrNr1i c nxio1nrsi s

Evidence in support of phylogenetic constraints on the
timing of owering was examined by looking at the
grouping of owering time and its temporal concentration
across families. Species within all families for which the
midpoint was calculated were split into wet season
(owering mid-point in December, January, February
Fig. 1 (a) The total number of species collected and (b) the number of those species recorded owering by month for the Wet
Tropics rain forest ora, North Queensland.
1
1
2
1

=

| | p p
ik jk
k
n
373

Rain forest
owering in
northern Australia

2006 The Authors
Journal compilation
2006 British
Ecological Society,

Journal of Ecology

94

, 369382

or March) and dry season owerers and a contingency
analysis performed. The contribution of higher taxo-
nomic division of plants, according to the phylogeny
reported in Bremer

et al

. (2000), to the timing of ow-
ering was tested using a heterogeneity

G

-test (Sokal &
Rohlf 1995). This phylogeny is based on recent cladistic
methods and the introduction of molecular sequence data.
Data were partitioned initially into Eudicots and Laurales.
The Eudicots were then further divided into Asterids,
Rosids and Monocots. Finally, heterogeneity was evalu-
ated among families within the Rosids and Asterids.
In order to determine if the timing of owering dif-
fered among species within genera and within families,
repeated measures analyses of variance were used.
Table 1 Index of owering overlap calculated for the 20 largest families that had at least eight species with a minimum of eight
records. The upper and lower limits of the 95% median of 1000 random simulations of overlap are shown. The distribution of
owering is classed as clumped for an overlap index above the 95% maximum and staggered if less than the 95% minimum
Family
No.
species
Actual overlap
index
95%
minimum
95%
maximum Distribution
Annonaceae 9 0.4277 0.2268 0.3444 Clumped
Apocynaceae 12 0.3833 0.3182 0.4121 Random
Celastraceae 10 0.3529 0.3319 0.3973 Random
Eleaeocarpaceae 18 0.2362 0.2190 0.2814 Random
Euphorbiaceae 53 0.3974 0.3508 0.3654 Clumped
Fabaceae 14 0.3502 0.3219 0.3878 Random
Lauraceae 51 0.3120 0.2266 0.2503 Clumped
Malvaceae 9 0.4208 0.3758 0.4580 Random
Meliaceae 12 0.2893 0.1971 0.2896 Random
Mimosaceae 17 0.3745 0.2542 0.3218 Clumped
Monimiaceae 8 0.2518 0.2323 0.3611 Random
Myrtaceae 65 0.3092 0.2775 0.2915 Clumped
Proteaceae 30 0.2363 0.2295 0.2628 Random
Rubiaceae 21 0.4648 0.3519 0.3922 Clumped
Rutaceae 32 0.3109 0.3011 0.3270 Random
Sapinaceae 38 0.2669 0.2420 0.2712 Random
Sapotaceae 9 0.3887 0.3570 0.4191 Random
Sterculiaceae 9 0.3495 0.2909 0.3580 Random
Verbenaceae 13 0.2955 0.2654 0.3229 Random
Table 2 Index of owering overlap calculated for those genera with at least ve species for which a minimum of eight records
existed. The upper and lower limits of the 95% median of 1000 random simulations of overlap are shown. The distribution of
owering is classed as clumped for an overlap index above the 95% maximum and staggered if less than the 95% minimum
Family Genus
No.
species
Actual mean
overlap
95%
minimum
95%
maximum Distribution
Clerodendrum Chlerodendrum 5 0.4682 0.2837 0.4831 Random
Combretaceae Terminalia 6 0.4495 0.2527 0.4405 Clumped
Elaeocarpaceae Elaeocarpus 14 0.2413 0.1825 0.2594 Random
Euphorbiaceae Croton 5 0.4483 0.3524 0.4881 Random
Mallotus 7 0.4434 0.3201 0.4373 Clumped
Phyllanthus 5 0.4695 0.3351 0.4688 Clumped
Lamiaceae Plectranthus 7 0.4815 0.3509 0.4553 Clumped
Lauraceae Beilschmiedia 7 0.2353 0.1225 0.3047 Random
Cryptocarya 22 0.3125 0.1922 0.2504 Clumped
Endiandra 19 0.3225 0.2144 0.2736 Clumped
Litsea 6 0.3279 0.1695 0.4322 Random
Meliaceae Dysoxylum 6 0.2476 0.1437 0.3606 Random
Mimosaceae Acacia 13 0.5297 0.2577 0.3506 Clumped
Myrtaceae Melaleuca 5 0.4389 0.2686 0.4690 Random
Rhodomyrtus 7 0.4815 0.3509 0.4572 Clumped
Syzygium 27 0.2739 0.2301 0.2655 Clumped
Pittosporaceae Pittosporum 5 0.4511 0.1187 0.3680 Clumped
Proteaceae Helicia 6 0.3297 0.2091 0.3258 Clumped
Rutaceae Acronychia 8 0.2967 0.2395 0.3611 Random
Flindersia 7 0.2994 0.2195 0.3824 Random
Sapotaceae Pouteria 10 0.3646 0.3262 0.4113 Random
Solanaceae Solanum 8 0.3542 0.2976 0.4091 Random
Symplocaceae Symplocos 9 0.3087 0.1762 0.3146 Random
374
S. L. Boulter,
R. L. Kitching &
B. G. Howlett
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
Months were treated as repeated measures, species as
subjects and the chosen taxonomic unit (family or
genus) as the grouping variables. A signicant inter-
action between month and taxa is taken to indicate that
the timing of owering was different among the chosen
taxa. Those families with three or more species with a
minimum of 10 owering records, and those genera
with two or more species with a minimum of 10 owering
records were used for the analysis. Due to the size of the
data sets the family and genera data were analysed
separately. The Huynh-Feldt Epsilon correction was
used to adjust the degrees of freedom.
Using a KruskalWallis test, mean vector length or
owering concentration (equation 2) was compared for
species among families to test if owering intensity was
inuenced by membership.
Results
The results of this study have generated data at the spe-
cies level, represented by the species mean vectors, and
two types of community-level data, the number of spe-
cies owering each month and the number of species
with mean vectors falling in each month, which are
summarized for the entire ora.
cii x:1r nxio1nrsrs
Records for 1371 species from 118 families and 533 genera
were examined. Thirty-three of the families were rep-
resented by a single species. The family Myrtaceae, in
contrast, was represented by 129 species. The number
of species with a peak of owering within a month and
the total number of species owering in a month were
non-randomly distributed across the course of the year
(Runs test, P = 0.011). November had the highest
number of species owering in any month with over
600 species owering (Fig. 1b). October, December
and January were also months of high owering whilst
the lowest number was recorded for April, and July and
August are also months of low activity.
Using the calculated owering midpoint for all spe-
cies for which we had 10 or more owering records, 75
of 511 species had peak owering in November
(Fig. 2). Both owering activity and calculated peak
owering therefore showed a general trend of increasing
in the lead up to the wet season, peaking in November
and continuing for many species into the rst half of the
wet season. The lowest number of species displaying
any owering activity occurred at the end of the wet
season (March), although this was followed by a small
peak in owering during April and May.
The general pattern differs between the two geographical
regions (Fig. 3). Flowering in the more tropical north
reects a similar trend to that seen for all species across
the entire region, with a distinct peak in October
through to December, and the remainder of the year
uctuating around the same, lower level (Fig. 3a). The
south, however, increases from a low period through
June to August to a distinct peak at the start of the wet
season and then a gradual decrease (Fig. 3b). Runs
tests show that both the north and south patterns
represent very strong evidence against randomness and
thus indicate seasonal increasing and decreasing trends
(P < 0.01).
Flowering in the northern zone demonstrated greater
variation with altitude. Both the upland and highland
zones showed a peak in owering at the start of the wet
season, with the proportion of species owering in
highland areas showing a dramatic increase in ower-
ing activity in October/November. In contrast, in the
lowland areas, activity increased only slightly across
Fig. 3 Flowering midpoint for species recorded (a) north of 17 and (b) south of 17 in the Wet Tropics of northern Australia.
Fig. 2 The distribution of mean owering times (peak
owering) calculated as an algebraic vector.
375
Rain forest
owering in
northern Australia
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
June and July (the dry season) and again in October
(just before the start of the wet season) (Fig. 4a). Runs
tests were still signicantly different from random
( P < 0.05) when tested across the altitudinal groups.
Flowering in the south shows a similar pattern at all
altitudes (Fig. 4b) although only the Uplands records
show a signicant seasonal trend when tested with the
Runs test (P < 0.01). The greater number of species
found at lowland sites may be the result of collecting
bias, as these rain forests are more accessible and of
greater current extent than their higher counterparts.
ni o1i c nxio1nrsrs
Analyses of owering overlap between species within
19 of the 20 largest families were conducted. Moraceae
was excluded as only one of its 21 species had the min-
imum number of records required. Of the remaining
19 families, Lauraceae, Euphorbiaceae, Myrtaceae,
Mimosaceae, Rubiaceae and Annonaceae demon-
strated an observed mean overlap greater than 97.5%
of the simulated values (Table 1). Flowering for species
within these families across the entire Wet Tropics
appears to be aggregated. In contrast, no family for
which the observed mean overlap was calculated,
demonstrated a value less than 97.5% of the simulated
values and therefore no families demonstrated the
staggered owering distribution predicted by the
pollinator competition hypothesis. Our results show a
trend of clumped owering patterns in the more speci-
ose families but this relationship is not signicant
(logistic regression, P > 0.05). Groups of species with
more records were not more likely to be signicantly
non-random than those with fewer records. Eighteen
of the 19 families tested were stratied according to
species number and retested (Moniaceae did not have
sufcient species with greater than 14). The results
remained the same, except for four families when spe-
cies with greater than 20 records were used, with two
showing signicant clumping, and two no longer show-
ing a signicant result. We conclude that increasing the
minimum number of records used does not increase the
chances of a signicant result.
At the generic level, 25 genera had at least ve species
with sufcient owering records and Acacia, Cryptocarya,
Endiandra, Mallotus, Phyllanthus, Pittosporum, Plec-
tranthus, Syzygium, Terminalia, Helicia and Rhodomyrtus
showed that owering was aggregated for species
(Table 2). Again, there was no evidence of staggered
distributions of owering times at the generic level.
Using the null model technique described for
the pollinator competition model, species within
the families Myrtaceae, Lauraceae, Sapindaceae and
Euphorbiaceae were analysed according to the bio-
geographical unit (combined latitude and altitude of
collection) in which the records were made. Some
variation was evident among units (Table 3). Species
recorded for Myrtaceae in the south showed a clumped
distribution, whereas in the north their owering over-
lap could not be distinguished from random. When
further subdivided into altitudinal categories, only the
highland species in the south showed any deviation
from random, having an aggregated distribution. In
contrast, species in the family Sapindaceae showed a
staggered distribution in the south, although this trend
was not reected in data when further divided into alti-
tudinal categories.
1nr inxiocrNr1i c nxio1nrsi s
The Annonaceae were excluded from the heterogeneity
analysis as this was the only family representing the
higher clade, Magnoliales. In this instance, it would be
impossible to determine if heterogeneity occurs within
or among the higher clade. When owering midpoints
were divided into wet and dry season owering, a
number of families owered exclusively in one season
(Oleaceae, Combretaceae and Annonaceae in the wet
and Pittosporaceae, Caesalpiniaceae and Capparaceae
in the dry season), while other families appeared to
be dominated by either wet or dry season owering
(Table 4). Not surprisingly, the distribution of ower-
ing across seasons varied signicantly among families
(G
Hf
= 122.01, d.f. = 38, P < 0.001). There was signi-
cant heterogeneity among families within the Asterids
and Rosids (Table 5). The majority of families within
Fig. 4 Proportion of species recorded owering by month at the altitudinal categories lowland (0400 m), upland (400800 m)
and highland (> 800 m) for rain forest (a) north of 17 and (b) south of 17 in the Wet Tropics of northern Australia.
376
S. L. Boulter,
R. L. Kitching &
B. G. Howlett
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
each of these higher clades showed dominance of one
or other season (Table 4), but there was no consistent
pattern of owering peaks within each clade. Further,
when Asterids and Rosids were compared within the
yet higher clade, the Eudicotyledones, no signicant
difference was indicated.
We also showed (Fig. 5) that there was no signicant
relationship between similarity in owering patterns
(as indicated by correlation coefcients based on the
number of owering records each month) and the
phylogenetic distances among those families showing
clumped distributions of owering (as determined in
our tests of the biotic hypothesis).
The number of owering records differed signicantly
among months and among taxa, for both genera and
families (repeated measures :Nov:, P < 0.0001, Table 6).
This result is reected in the observed patterns of increased
owering at the end of the dry/beginning of the wet season.
At both the generic and family level, there is a sig-
nicant difference in owering rates for species within
these taxonomic groupings by month (within- and
between-species interaction, Table 6), which accords
with the predictions of the phylogenetic hypothesis.
Duration and intensity of owering, measured as
owering concentration, and indicated by the mean
lengths of the owering vectors, also differed signicantly
among families (KruskalWallis test statistic = 143.67,
d.f. = 41, P < 0.0001). The families, Lauraceae, An-
nonaceae and Anacardiaceae had the highest mean
vector lengths (Table 7), with species owering intensely
over short time periods. Species within the families
Table 3 Index of owering overlap calculated for the four largest families divided into individuals recorded north of 17 and south
of 17 and at altitudes < 400 m (lowlands), 400800 m (uplands) and > 800 m (highlands)
Family Latitude Altitude
No.
species
Actual
overlap
95%
minimum
95%
maximum Distribution
Myrtaceae North All 23 0.2987 0.2688 0.3090 Random
Lowlands 13 0.2006 0.1610 0.2344 Random
Uplands 4 0.1952 0.0714 0.4000 Random
Highlands 11 0.2531 0.1753 0.2628 Random
South All 46 0.2791 0.2474 0.2659 Clumped
Lowlands 15 0.1735 0.1337 0.2049 Random
Uplands 15 0.1868 0.1354 0.2070 Random
Highlands 13 0.2367 0.1600 0.2355 Clumped
Lauraceae North All 30 0.2504 0.1791 0.2134 Clumped
Lowlands 10 0.2273 0.1231 0.2236 Clumped
Uplands 5 0.2701 0.1126 0.3645 Random
Highlands 7 0.2578 0.1286 0.3147 Random
South All 37 0.3238 0.2078 0.2439 Clumped
Lowlands 19 0.2119 0.1558 0.2143 Random
Uplands 18 0.2990 0.1209 0.1871 Clumped
Highlands 21 0.2322 0.1222 0.1793 Clumped
Euphorbiaceae North All 34 0.2983 0.2547 0.2804 Clumped
Lowlands 17 0.2711 0.2241 0.2790 Random
Uplands + Highlands 5 0.2776 0.1689 0.3439 Random
South All 36 0.3743 0.3100 0.3343 Clumped
Lowlands 14 0.2383 0.1663 0.2346 Clumped
Uplands 14 0.2383 0.1653 0.2417 Random
Highlands 6 0.2459 0.1289 0.2889 Random
Sapindaceae North All 21 0.2258 0.1703 0.2285 Random
Lowlands 5 0.1933 0.0883 0.3200 Random
Uplands + Highlands 5 0.2122 0.1622 0.4689 Random
South All 39 0.1916 0.1917 0.2226 Staggered
Lowlands 9 0.2333 0.1486 0.3015 Random
Uplands + Highlands 22 0.1610 0.1471 0.1925 Random
Fig. 5 Phylogenetic distance vs. the correlation coefcient of
owering per month for each pair of the ve families that
demonstrated a signicantly clumped distribution (Table 1).
377
Rain forest
owering in
northern Australia
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
Annonaceae and Anacardiaceae all owered in 7 or
less months of the year. Of the 51 species from the
family Lauraceae used in the analysis, 48 owered in
7 months and 28 (more than half) owered in
4 months of the year. Families with low mean r-values
included the Dilleniacae, Thymelaeaceae and Epacri-
daceae (Table 7). Flowering across species in these
families was of similar intensity across at least 8 months.
We conclude that there may well be a phylogenetic
dimension to coincidence of owering of species within
genera and families. There is, however, no convincing
evidence of this at higher levels.
Discussion
coxxiNi 1x-irvri, sr:soN:i i:11rNs
Community-level owering in the Wet Tropics of
Australia shows a distinct annual rhythm, with many
species at peak owering near the beginning of the wet
season. Synchrony of owering associated with cli-
matic variation is a widespread phenomenon (Frankie
et al. 1974; Morellato et al. 2000). While there is a large
diversity of phenological patterns amongst trees of
seasonally dry tropical forests, late dry-season ower-
ing is common (Frankie et al. 1974; Heideman 1989;
Borchert 1994; Ramrez 2002; Borchert et al. 2004).
Climactic changes are known proximate cues of vege-
tative phenology, and this, taken together with the fact
that vegetative phenology is a strong determinant of
Table 4 Number of species whose calculated owering peak falls in the wet or dry season in each family
Number of species
Order Family Dry Wet
Eumagnoliids Magnoliales Annonaceae 0 6
Eudicots Proteales Proteaceae 15 11
Eudicots Asterids Apiaceae Araliaceae 1 4
Eudicots Asterids Apiales Pittosporaceae 6 0
Eudicots Asterids Ericales Epacridaceae 2 2
Eudicots Asterids Ericales Myrsinaceae 4 1
Eudicots Asterids Ericales Sapotaceae 2 6
Eudicots Asterids Gentianales Apocynaceae 3 6
Eudicots Asterids Gentianales Rubiaceae 7 11
Eudicots Asterids Lamiales Acanthaceae 4 1
Eudicots Asterids Lamiales Lamiaceae 6 1
Eudicots Asterids Lamiales Oleaceae 0 5
Eudicots Asterids Lamiales Verbenaceae 2 2
Eudicots Asterids Solanales Boraginaceae 2 2
Eudicots Asterids Solanales Solanaceae 5 1
Eudicots Rosids Elaeocarpaceae 6 5
Eudicots Rosids Brassicales Capparaceae 4 0
Eudicots Rosids Celastrales Celastraceae 3 5
Eudicots Rosids Fabales Caesalpiniaceae 5 0
Eudicots Rosids Fabales Fabaceae 9 4
Eudicots Rosids Fabales Mimosaceae 12 2
Eudicots Rosids Malpghiales Flacourtiaceae 1 4
Eudicots Rosids Malpighiales Euphorbiaceae 15 28
Eudicots Rosids Malvales Malvaceae 5 1
Eudicots Rosids Malvales Sterculiaceae 7 2
Eudicots Rosids Malvales Thymelaeaceae 3 1
Eudicots Rosids Myrtales Combretaceae 0 6
Eudicots Rosids Myrtales Myrtaceae 38 17
Eudicots Rosids Oxalidales Cunoniaceae 4 1
Eudicots Rosids Rosales Rhamnaceae 6 2
Eudicots Rosids Rosales Rosaceae 3 1
Eudicots Rosids Sapindales Anacardiaceae 3 2
Eudicots Rosids Sapindales Meliaceae 6 2
Eudicots Rosids Sapindales Rutaceae 16 12
Eudicots Rosids Sapindales Sapindaceae 18 10
Eudicots Rosids Saxifragales Grossulariaceae 4 1
Laurales Laurales Monimiaceae 2 2
Laurales Laurales Lauraceae 8 36
Table 5 The contribution of higher taxa to the heterogeneity
of owering season (dry or wet)
G d.f. P
Eudicots vs. Laurales 32.52213293 1 < 0.0001
Asterids vs. Rosids 2.558949257 1 NS
Families (Asterids) 31.8672054 13 < 0.0001
Families (Rosids) 49.53998932 19 < 0.0001
378
S. L. Boulter,
R. L. Kitching &
B. G. Howlett
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
owering time in seasonally dry forests (Borchert et al.
2004), suggests seasonal climate variation should be an
important determinant of community level owering
patterns.
At the community level, peak owering coincides
with the passage of the sun directly over the Wet Trop-
ics. This meets the predictions of van Schaik et al.
(1993) and Wright & van Schaik (1994) that peak ower-
ing along a latitudinal gradient closely tracks the
position of the sun. Maximal irradiance coincides with
the rst month for which average rainfall exceeds
60 mm and the strong selective pressure on phenology
that this combination is expected to exert appears to be
reected in community-wide owering patterns.
When the owering records were partitioned into
latitudinal categories, the south, despite a similar
seasonal trend to the whole community, had a longer
peak owering season, extending throughout the
entire wet season. When the data were further parti-
tioned into altitudinal categories, the trend for
increased owering activity at the end of the dry season
accentuated with increased elevation. The owering
patterns of the northern lowlands differed considerably
from that of overall wet-season domination as seen
across the entire ora. Variation in owering patterns
with changes in latitude and altitude provides secondary
evidence for the inuence of variations in environmental
factors.
The coincidence of owering with seasonal environ-
mental variation also coincides with increased pollin-
ator activity, especially of insects, and it might be argued
that climate is both a proximate cue and an ultimate
cause of owering patterns. Certainly insect abundance
and biomass peaks during the wet season at an upland
site within the Wet Tropics have been correlated with
seasonal increases in resources such as owers, new
leaves and fruit (Frith & Frith 1985). Whether the co-
incidence of greatest insect activity with owering
activity is a cause or an effect, however, remains a moot
point (Rathcke & Lacey 1985).
Table 6 Results of a repeated measures :Nov: of monthly owering within (a) genera and (b) families
Source Sum-of-squares d.f. Mean square F P-value
(a) Monthly owering within genera
Between species
Genus 1227.46 115 10.67 1.57 < 0.01
Error 1977.67 290 6.82
Within species
Month 367.02 11 33.37 7.33 < 0.0001
Month genus 8679.31 1265 6.86 1.51 < 0.0001
Error 14517.07 3190 4.55
(b) Monthly owering within families
Between species
Family 1289.34 46 28.03 2.89 < 0.0001
Error 5106.08 526 9.71
Within species
Month 313.04 11 28.45 5.69 < 0.0001
Month family 4805.43 506 9.5 1.9 < 0.0001
Error 28924.18 5786 5
Table 7 The mean concentration of owering (r) for all
species by family
Family Mean r SE
Dilleniaceae 0.246 0.091
Thymelaeaceae 0.333 0.044
Epacridaceae 0.396 0.031
Boraginaceae 0.413 0.081
Celastraceae 0.417 0.076
Sapotaceae 0.428 0.056
Araliaceae 0.431 0.057
Grossulariaceae 0.446 0.170
Acanthaceae 0.456 0.078
Malvaceae 0.461 0.056
Euphorbiaceae 0.466 0.033
Lamiaceae 0.483 0.103
Solanaceae 0.498 0.046
Cunoniaceae 0.536 0.100
Rosaceae 0.557 0.086
Caesalpiniaceae 0.566 0.112
Sterculiaceae 0.567 0.089
Verbenaceae 0.587 0.081
Capparaceae 0.594 0.086
Rubiaceae 0.609 0.049
Rutaceae 0.619 0.040
Fabaceae 0.626 0.048
Combretaceae 0.628 0.076
Apocynaceae 0.631 0.053
Monimiaceae 0.637 0.059
Myrsinaceae 0.647 0.169
Pittosporaceae 0.667 0.088
Myrtaceae 0.668 0.028
Tiliaceae 0.669 0.075
Lecythidaceae 0.678 0.187
Symplocaceae 0.698 0.091
Flacourtiaceae 0.711 0.093
Mimosaceae 0.718 0.044
Rhamnaceae 0.722 0.063
Oleaceae 0.725 0.048
Proteaceae 0.737 0.036
Elaeocarpaceae 0.758 0.057
Meliaceae 0.759 0.058
Sapindaceae 0.765 0.030
Lauraceae 0.789 0.023
Annonaceae 0.790 0.036
Anacardiaceae 0.855 0.034
379
Rain forest
owering in
northern Australia
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
sirci rs irvri riovri Nc: ni o1i c o
inrNoioci c:i c:isrs
Asynchronous owering
Temporally segregated owering, the key prediction of the
pollinator competition hypothesis, was not demonstrated
for any group of congeners or confamilials across the
entire Wet Tropics of Australia (with one dubious exception
in the southern Sapindaceae). Strictly the staggered result
for individuals of the Sapindaceae found in the south could
be taken as an indication that they had evolved owering
patterns in an environment of pollinator scarcity. The
isolated nature of this result, both taxonomically and
regionally, leads us to treat this outcome with great
caution. There can be little doubt that, in general, our
analyses give little if any support to the hypothesis that
implies competition for pollination resources. This result
is not unexpected. Few studies have demonstrated such
divergence of owering times (Stiles 1975; Ashton et al.
1988; Wright & Calderon 1995; Borchsenius 2002). For
those that have, there is stronger evidence that staggered
owering may result from avoidance of interspecic pollen
transfer (Waser 1983) rather than pollinator competition.
Evidence that pollinators are a limiting resource is seldom
found (Rathcke & Lacey 1985). While owering time is
somewhat variable, if it is accepted that owering pheno-
logy is under strong phylogenetic constraints (Ollerton
& Lack 1992; cf. Rathcke & Lacey 1985), then other
premating isolating mechanisms may be more effective
in reducing interspecic competition and gene ow.
Wright & Calderon (1995) warned against interpreting low
evidence of staggering amongst species in a community-
wide study of owering on Barro Colorado Island,
Panama, as evidence against the shared pollinator hypo-
thesis. They suggested, as an alternative, that selection
to avoid pollinator competition simply does not obscure
phylogenetic patterns of owering. It could be argued
that random owering times may also lessen com-
petition for pollinators. If this is accepted, then the evo-
lution of asynchronous owering may not be necessary
for successful reproduction. In the present study, fail-
ure to demonstrate staggered owering times may also
reect the temporal and geographical scale at which
data have been collected and analysed. While staggered
owering of species has been shown across several
months (Rabinowitz et al. 1981), other authors have
found that, for many species, anthesis occurs over
a matter of days or weeks, rather than months (e.g.
Syzygium tierneyanum, Hopper 1980; Shorea spp., Yap
& Chan 1990; Shorea parvifolia, Sakai et al. 1999; Uvaria
elmeri, Nagamitsu & Inoue 1997). Asynchronous ower-
ing may be more difcult to detect in comparisons of
owering based on monthly analyses.
Synchronous owering
Evidence of synchronous or clumped owering among
particular taxa satises, at least in part, the predictions
of the climatic hypothesis, one version of the biotic
hypothesis, i.e. mass action and the phylogenetic
hypothesis. Separating the evidence in support of each
of these competing drivers is accordingly difcult. The
coincidence of a large number of species with seasonal
variation in climate suggests that at the least, environ-
mental factors cue phenological activity in a large
number of species. Separating the inuence of biotic
and phylogenetic factors, however, requires more data
than are currently available. This analysis could be
greatly enriched by knowledge of the pollinators of a
large number of species (currently for the Wet Tropics
we are aware of no more than 20 published studies of
pollination) and resolution of phylogeny to the level of
species. With this information, owering data could
be divided into actual pollinator groups and tech-
niques such as phylogenetically independent contrasts
(Felsenstein 1985; Harvey & Pagel 1991) could be used
to partition out the effect of phylogeny.
Our analysis thus far, has shown that the coincidence
of owering among the species of each family is limited,
with only ve of the 19 families examined being signi-
cantly clumped. Further, evidence of clumping was
more likely to be found among congeneric species and
often, but not always, in genera belonging to clumped
families. In addition, we demonstrated that species within
many families ower preferentially in the wet or dry
season. For example, peak owering for species of the
Lauraceae family was restricted to the period between
October and June, with over 80% of species at their
owering peak in the wet season. In contrast, 12 of the
14 species tested for Mimosaceae owered in the dry
season. In addition, several smaller families for which
the null hypothesis was not tested also showed a strong
wet or dry season dominance in owering (Tables 1 and
4). We note that while community-level data show
a seasonal peak in owering (suggesting climatic-
ally driven seasonality), when species are considered
community-wide, closely related species (i.e. confamilials)
exhibit clumped owering at times of the year other
than at the start of the wet season. This highlights the
variation in strategies adopted by plants. Again, we
emphasize that the physiology of individual plants, as
outlined by Borchert et al. (2004), will be an important
determinant in their response to environmental changes.
If the timing of owering (i.e. wet or dry season) or
coincidence of owering is a factor of phylogeny, then we
would expect that phylogenetic distance between families
would relate to the timing of owering. This was not the
case. For example, those species that showed clumping
often did so at different times of the year and seasonally
owering families showed little recent common ancestry.
We did show, however, that when grouped by genera
or family, the timing, duration and concentration of
owering, was consistent among members of particular
taxonomic groups (i.e. family or genera). Similar results
have been found from other oras (Wright & Calderon
1995; Bawa et al. 2003), although Bawa et al. (2003),
analysing owering among confamilial species, found
380
S. L. Boulter,
R. L. Kitching &
B. G. Howlett
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
that while phylogeny appeared to constrain the fre-
quency of owering (i.e. annual, supra annual), timing
and duration of owering were not so constrained. We
conclude that any possible phylogenetic element of
owering patterns, in the case of the Wet Tropics of
Australia, is restricted to the level of family or genus.
For plants that rely on the transfer of pollen between
individuals, the inuence of owering time on success
has led to a common expectation that this trait should
be subject to selection. The evidence that plant species
in the Wet Tropics of Australia, at least at the level
of genus and family, show some relationship between
taxonomy and owering phenology may be evidence
of this selection. Closely related species demonstrate
considerable morphological similarity, however, and
morphological characters of owers, such as size, shape,
scent and nectar production will determine the attrac-
tion and success of pollinators. While the operation of
biotic selection and phylogenetic conservancy is
impossible to clearly distinguish, it may not make sense
to try. It is not unreasonable to expect that evolution
generates patterns of trait variation that are both cor-
related with phylogeny and maintained by selective
forces, in this case biotic pollinators (Westoby et al.
1995). Bolmgren et al. (2003) argue that a lack of clear
evidence of biotic inuences cannot simply be assumed
to demonstrate phylogenetic conservancy (cf. Ollerton
& Lack 1992), and we would agree with this position
and the corollary.
Distinction between the relative inuence of phylo-
geny and proximate factors may rely on secondary
evidence. For example, if phylogenetic constraints are
stronger than local pressures, then species of a family
should ower at similar times regardless of their geo-
graphical location. In addition, owering times across
families should more or less coincide depending upon
their taxonomic afnities, particularly within orders
(Kochmer & Handel 1986). In contrast, if causal rela-
tionships between abiotic factors and phenology exist
(i.e. seasonality is simply climate driven) then timing
and duration of owering should vary among indi-
viduals of a species collected at different geographical
locations (Borchert 1996), and increased latitudes (van
Schaik et al. 1993) and altitude (Burger 1974). As dis-
cussed above, community-level owering patterns were
certainly inuenced by increases in latitude, although
increased altitude simply accentuated the peaks and
troughs. Whatever the alternate explanation, the vari-
ation of owering patterns with increased latitude and
altitude supports the notion that, where abiotic pro-
cesses favour phenological convergence (in this case
different rainfall and temperature gradients), it is the
strength of these processes that determine the shape
or pattern of owering trends.
n:1: coNs1:i N1s
This analysis is based on extensive herbarium records.
Accordingly the data may reect collecting biases. Few
studies have utilized herbarium records or other mass
collections to supplement phenological information
derived from direct observation in the eld (e.g. Burger
1974; Croat 1975; Wright & Calderon 1995; Borchert
1996). Flowering periods derived from herbarium
records, although in some cases longer, have been demon-
strated to reect those from eld surveys (Borchert
1996). The Atherton herbarium from which these data
were principally compiled has samples from over
100 years of collecting and contains substantial collec-
tions made within ecologically or biogeographically
motivated surveys. In this case, the collection provides
an extensive knowledge of owering for a large propor-
tion of species found across the Wet Tropics, for which
there are few published eld studies. Data from two
separate studies, from one lowland and one upland site,
recorded peak owering in SeptemberOctober from
4 years of data (Hopkins & Graham 1989), and Octo-
ber and January in two consecutive years (Frith & Frith
1985). These studies offer results not dissimilar to the
conclusion here that peak owering occurs on average
in the period of OctoberNovember. We show that
there is little similarity between collecting patterns and
owering pattern, with the owering data showing a
marked increase in activity at the end of the dry season,
not reected in collecting data (Fig. 1), and conclude
that the herbarium data are a fair reection of ower-
ing patterns.
Studies conducted at the species and population
levels can show wide variation in owering patterns
(Sakai 2002), with annual rhythms observed at the
community level not reected by all individual species
(Newstrom et al. 1994). We suggest that the results of
the current study encompass the variation between
years detected in eld studies and represent general
regional rather than strictly local patterns. The clear
disadvantage of herbaria in the current study is that
supra-annual owering will not be detected. This may
be especially important when considering asynchro-
nous owering, as different mast owering species may
simply not ower in the same year, even if they do so at
the same time of year.
nrii Nr:1i Nc 1nr rvi nrNcr: soxr
coNciisi oNs
The precise timing of owering by individual plants
and species is likely to be the result of a combination of
abiotic, biotic and evolutionary factors. Distinguishing
the ultimate and proximate causes of phenological
events is difcult and interpretation of community-
level patterns in particular must be made with caution.
We have shown here that the ora of the Queensland
Wet Tropics shows a diversity of owering patterns,
although a general peak in activity coincides with the
end of the dry season/start of the wet season. Whether
thought to be the result of phylogenetic constraints or
pollinator association, coincidence of owering pat-
terns is particular only to each individual family at
381
Rain forest
owering in
northern Australia
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
best. Like a number of proceeding community studies
(e.g. Wright & Calderon 1995; Bawa et al. 2003), the
structure of community owering patterns of the
Australian Wet Tropics ora is unresolved. Precise
partitioning between phylogenetic, biotic and abiotic
factors is not possible. Different species respond differ-
ently to a variety of factors, and the inuence of factors
on the owering behaviour of individual species is
likely to represent a continuum across the ora.
Acknowledgements
We are grateful to the Rainforest CRC for nancial
support. We would like to thank Dr Bernie Hyland, Mr
Bruce Gray and Ms Rebel Elick for allowing us access
to the Atherton Herbarium specimens and assistance
at the Herbarium. We also thank Ms Nat Simpson for
assistance with data collection. Dr James McBroom
and Mr Alex Creagh provided advice and assistance
with the data analysis. Dr John Kanowski and Mr Rod
Eastwood are thanked for their patient and helpful dis-
cussions of the data analysis. We offer special thanks to
Dr Joe Wright for helpful comments on the rst draft,
and to Dr Kamal Bawa and an anonymous referee
whose thoughtful comments on a later draft greatly
improved this manuscript.
References
Ashton, P.S., Givish, T.J. & Appanah, S. (1988) Staggered
owering in the Dipterocarpaceae: new insights into oral
induction and the evolution of mast fruiting in the asea-
sonal tropics. American Naturalist, 132, 4466.
Batschelet, E. (1981) Circular Statistics in Biology. Academic
Press, London.
Bawa, K.S., Kang, H. & Grayum, M.H. (2003) Relationships
among time, frequency, and duration of owering among
tropical rain forest trees. American Journal of Botany, 90,
877887.
Bolmgren, K., Eriksson, O. & Linder, H.P. (2003) Contrast-
ing owering phenology and species richness in abiotically
and biotically pollinated angiosperms. Evolution, 57, 2001
2011.
Borchert, R. (1983) Phenology and control of owering in
tropical trees. Biotropica, 15, 8189.
Borchert, R. (1994) Soil and stem water storage determine
phenology and distribution of tropical dry forest trees.
Ecology, 75, 14371449.
Borchert, R. (1996) Phenology and owering periodicity of
Neotropical dry forest species: evidence from herbarium
collections. Journal of Tropical Ecology, 12, 6580.
Borchert, R., Meyer, S.A., Felger. R.S. & Porter-Bollard, L.
(2004) Environmental control of owering periodicity in
Costa Rican and Mexican tropical dry forests. Global Ecology
and Biogeography, 13, 409425.
Borchsenius, F. (2002) Staggered owering in four sympatric
varieties of Geonoma cuneata (Palmae). Biotropica, 34,
603606.
Bremer, K., Bremer, B. & Thulin, M. (2000) Introduction to
Phylogeny and Systematics of Flowering Plants, 6th edn.
Department of Systematic Botany, Evolution Biology
Centre, Uppsala University, Uppsala.
Burger, W.C. (1974) Flowering periodicity at four altitudinal
levels in eastern Ethiopia. Biotropica, 6, 3842.
Croat, T.B. (1975) Phenological behaviour of habit and hab-
itat classes on Barro Colorado Island (Panama Canal
Zone). Biotropica, 7, 270277.
Davies, S.J. & Ashton, P.S. (1999) Phenology and fecundity in
11 sympatric pioneer species of Macaranga (Euphor-
biaceae) in Borneo. American Journal of Botany, 86, 1786
1795.
Felsenstein, J. (1985) Phylogenies and the comparative
method. American Naturalist, 125, 115.
Frankie, G.W., Baker, H.G. & Opler, P.A. (1974) Com-
parative phenological studies of trees in tropical wet and dry
forests in the lowlands of Costa Rica. Journal of Ecology,
62, 881919.
Frith, C.B. & Frith, D.W. (1985) Seasonality of insect abund-
ance in an Australian upland tropical rainforest. Australian
Journal of Ecology, 10, 237248.
Graham, E.A., Mulkey, S.S., Kitajima, K., Phillips, N.G. &
Wright, S.J. (2003) Cloud cover limits net CO
2
uptake and
growth of a rainforest tree during tropical rainy seasons.
Proceedings of the National Academy of Sciences of the
USA, 100, 572576.
Hamann, A. (2004) Flowering and fruiting phenology of a
Philippine submontane rain forest: climatic factors as pro-
ximate and ultimate causes. Journal of Ecology, 92, 2431.
Harvey, P.H. & Pagel, M.D. (1991) The Comparative Method
in Evolutionary Biology. Oxford University Press, Oxford.
Heidemann, P.D. (1989) Temporal and spatial variation in the
phenology of owering and fruiting in a tropical rainforest.
Journal of Ecology, 77, 10591079.
Hopkins, M.S. & Graham, A.W. (1989) Community pheno-
logical patterns of a lowland tropical rainforest in north-
eastern Australia. Australian Journal of Ecology, 14, 399
413.
Hopper, S.D. (1980) Pollination of the rain-forest tree
Syzygium tierneyanum (Myrtaceae) at Kuranda, Northern
Queensland. Australian Journal of Botany, 28, 223237.
Hyland, B.P.M., Whifn, T., Christophel, D.C., Gray, B.,
Elick, R.W. & Ford, A.J. (1999) Australian Tropical Rain
Forest Trees and Shrubs. CSIRO Publishing, Melbourne,
Australia.
Johnson, S.D. (1992) Climatic and phylogenetic determinants
of owering seasonality in the Cape Flora. Journal of Ecol-
ogy, 81, 567572.
Kochmer, J.P. & Handel, S.N. (1986) Constraints and compe-
tition in the evolution of owering phenology. Ecological
Monographs, 56, 303325.
Morellato, L.P.C., Talora, D.C., Takahasi, A., Becke, C.C.,
Romera, E.C. & Zipparro, V.B. (2000) Phenology of Atlantic,
forest trees: a comparative study. Biotropica, 32, 811823.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da
Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for
conservation priorities. Nature, 403, 853858.
Nagamitsu, T. & Inoue, T. (1997) Cockroach pollination
and breeding system of Uvaria elmeri (Annonaceae) in a
lowland mixed-dipterocarp forest in Sarawak. American
Journal of Botany, 84, 208213.
Newstrom, L.E., Frankie, G.W., Baker, H.G. & Colwell, R.K.
(1994) Diversity of long-term owering patterns. La Selva.
Ecology and Natural History of a Neotropical Rain Forest
(eds L.A. McDade, K.S. Bawa, H.A. Hespenheide & G.S.
Hartshorn), pp. 142160. The University of Chicago Press,
Chicago.
Nix, H.A. & Switzer, M.A. (1991) Rainforest Animals: Atlas
of Vertebrates Endemic to Australias Tropics. Kowari 1 (ed.
J. Walker), pp. 6191. Australian National University,
Canberra.
Ollerton, J. & Lack, A.J. (1992) Flowering phenology, an
example of relaxation of natural selection? Trends in Ecology
and Evolution, 7, 274276.
Pleasants, J.M. (1980) Competition for bumblebee pollinators
in Rocky Mountain plant communities. Ecology, 61, 1446
1459.
382
S. L. Boulter,
R. L. Kitching &
B. G. Howlett
2006 The Authors
Journal compilation
2006 British
Ecological Society,
Journal of Ecology
94, 369382
Pleasants, J.M. (1990) Null-model tests for competitive
displacement: the fallacy of not focusing on the whole
community. Ecology, 71, 10781084.
Primack, R.B. (1985) Patterns of owering phenology in
communities, populations, individuals, and single owers.
The Population Structure of Vegetation (ed. J. White),
pp. 571593. Dr W. Junk, Dordrecht.
Rabinowitz, D., Rapp, J.K., Sork, V.L., Rathcke, B.J., Reese,
G.A. & Weaver, J.C. (1981) Phenological properties of
wind- and insect-pollinated prairie plants. Ecology, 62, 49
56.
Ramrez, N. (2002) Reproductive phenology, life-forms, and
habitats of the central plain. American Journal of Botany,
89, 836842.
Rathcke, B. (1983) Competition and facilitation among
plants for pollination. Pollination Biology (ed. L. Real),
pp. 305329. Academic Press, Orlando.
Rathcke, B.J. & Lacey, E.P. (1985) Phenological patterns in
terrestrial plants. Annual Review of Ecology and System-
atics, 16, 179214.
Sakai, S. (2002) General owering in lowland mixed Dipterocarp
forests of South-east Asia. Biology Journal of the Linnean
Society, 75, 233247.
Sakai, S., Momose, K., Yumoto, T., Kato, M. & Inoue, T.
(1999) Beetle pollination of Shorea parvifolia (section
Mutica, Dipterocarpaceae) in a general owering period in
Sarawak, Malaysia. American Journal of Botany, 86, 6269.
Sattler, P.S. & Williams, R.D. (1999) The Conservation Status
of Queenslands Bioregional Ecosystems. Environmental
Protection Agency, Brisbane, Australia.
Schneider, C. & Moritz, C. (1999) Rainforest refugia and
evolution in Australias Wet Tropics. Proceedings of the
Royal Society of London, 266, 191196.
Sokal, R.R. & Rohlf, F.J. (1995) Biometry. The Principles and
Practice of Statistics in Biology Research, 3rd edn. W.H.
Freeman, San Francisco.
Stiles, G.F. (1975) Ecology, owering phenology, and
hummingbird pollination of some Costa Rican Heliconia
species. Ecology, 56, 285301.
Tracey, J.G. (1982) The Vegetation of the Humid Tropical
Region of North Queensland. CSIRO Publishing, Mel-
bourne, Australia.
van Schaik, C.P., Terborgh, J.W. & Wright, S.J. (1993) The
phenologogy of tropical forests: adaptive signicance and
consequences for primary consumers. Annual Review of
Ecology and Systematics, 24, 353377.
Waser, N.M. (1979) Pollinator availability as a determinant of
owering time in Ocotillo (Fouquieria splendens). Oecolo-
gia, 39, 107121.
Waser, N.M. (1983) The adaptive nature of oral traits: ideas
and evidence. Pollination Biology (ed. L. Real), pp. 241
285. Academic Press, New York.
Westoby, M., Leishman, M.R. & Lord, J.M. (1995) On
misinterpreting the phylogenetic correction. Journal of
Ecology, 83, 531534.
Winter, J.W. (1997) Responses of non-volant mammals to
late quaternary climatic changes in the Wet Tropics region
of North-eastern Australia. Wildlife Research, 24, 493
511.
Wright, S.J. (1996) Phenological responses to seasonality in
tropical forest plants. Tropical Forest Plant Ecophysiology
(eds S.S. Mulkey, R.L. Chazdon & A.P. Smith), pp. 440
460. Chapman & Hall, New York.
Wright, S.J. & Calderon, O. (1995) Phylogenetic patterns
among tropical owering phenologies. Journal of Ecology,
83, 937948.
Wright, S.J. & Cornejo, F.H. (1990) Seasonal drought and leaf
fall in a tropical forest. Ecology, 71, 11651175.
Wright, S.J. & van Schaik, C.P. (1994) Light and phenology of
tropical trees. American Naturalist, 143, 192199.
Yap, S.K. & Chan, H.T. (1990) Phenological behaviour of
some Shorea species in peninsular Malaysia. Reproductive
Ecology of Tropical Forest Plants (eds K.S. Bawa & M. Hadley),
pp. 2135. UNESCO, Paris.
Received 17 April 2005
revision accepted 27 September 2005
Handling Editor: David Burslem