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A New Classification for Plant Phenology Based on Flowering Patterns in Lowland Tropical

Rain Forest Trees at La Selva, Costa Rica


Author(s): L. E. Newstrom, G. W. Frankie and H. G. Baker
Reviewed work(s):
Source: Biotropica, Vol. 26, No. 2 (Jun., 1994), pp. 141-159
Published by: The Association for Tropical Biology and Conservation
Stable URL: http://www.jstor.org/stable/2388804 .
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BIOTROPICA 26(2): 141-159

1994

A New ClassificationforPlantPhenologyBased on Flowering


Patternsin LowlandTropicalRain ForestTrees at
La Selva, Costa Rica1
L. E. Newstrom and G. W. Frankie
of California,Berkeley,California94720, U.S.A.
Departmentof Entomology,University
and
H. G. Baker
of California,Berkeley,California94720, U.S.A.
Departmentof IntegrativeBiology,University

ABSTRACT
forplant phenologyare proposedto resolveproblemsin describing
A new classification
and conceptualframework
in 254 lowlandtropicalrain foresttreesof 173 species
tropicalpatterns.A long-term(12 yr) surveyof flowering
and complexpatterns.Analysis
fromthe La Selva BiologicalStationin Costa Rica showedhighlydiverse,irregular,
methodsratherthan
of this surveydata reliedprimarilyon graphicalanalysesthat provide data representation
differsfrompreviousones in three
numericalsummariesthat providedata reductionmethods.The classification
of the time series,based on explicittime and amplitudescales,so
frequency
ways. It uses, as the primarycriterion,
that irregular
temporalsequencesare revealed.It featuresa systemof subsidiaryclassesbased on otherquantitative
separatespatterns
Finally,theconceptualframework
duration,amplitude,date,and synchrony.
descriptors:
regularity,
at each level of analysisso thatadding the time seriesat one levelproducesa time seriesforthe nexthigherlevel.
Levels are hierarchical
fromthe flowerto the individual,population,and communitywith additionalnon-nested
levels such as the guild. The fourbasic classes-continual,subannual,annual, and supra-annual--areapplied to
forquantitativedescription
systemprovidesa logical framework
patternsat any level of analysis.The classification
of phenologicalbehaviorleadingto morestandardizedcomparisons.Thus we can see thattropicalphenologydiffers
fromtemperatephenologyin two majorways. In tropicalspecies,the natureof the patternmay changefromone
levelof analysisto the next,whichis not typicalof temperatespecies.In manytropicalspecies,phenologicalpatterns
varymorewidelyoverthe geographicrangeof a speciesthan theydo in temperatespecies.
guild; individual;La Selva BiologicalStation;lowlandtropicalrain
community;
Keywords: classification;
flowering;
population;tropicaltrees.
forest;phenology;

tropicalphenologyhas
temperatezone. In contrast,
discipline,in
beenan impreciseand oftenconfusing
littlestudiedand
partbecauseit has been relatively
in partbecauseit has beenhandicappedby thelack
termsand methods.Thispaperproofstandardized
and conceptualframework
posesa newclassification
thatprovidesa logicalsystemforquantitativedeapproachtopheA typological
scription
ofpatterns.
patternsthat may repnologynot only identifies
but also providesa unit
resentadaptivesyndromes
of analysisthatservesas a contextfororganizing
The systemcan be used forany reinformation.
curringeventin plant or animal lifecyclesin any
regionof theworld.We have developedit hereon
patternsin lowlandtropical
the basis of flowering
treesbutanyotherphenologicalcharacter
rainforest
(e.g., leafingor fruiting).
can be substituted
Most ofthephenologicalworkin lowlandtrophas beenconductedat thecommunity
icalrainforest
of the forest,
I Received 7 October 1992; revisionaccepted 4 June level to show the overallseasonality
cycles
fruiting
oftenwiththegoal of understanding
1993.

PLANT PHENOLOGY IS CONCERNED withthetimingof


events,and in particularis poorlyknown
recurring
species,althoughthis
forlowlandtropicalrainforest
of phenological
has thegreatestdiversity
ecosystem
patterns.The paucityof knowledgebeliesthe imtheecology
portanceofphenologyforunderstanding
and evolutionof speciesand communitiesin the
cyclesaftropics.The timingof plantreproductive
fectsnot onlyplantsbut also animalsthatdepend
on plant resources.It impingeson plant-plantinsuch as competitionforresourcesor for
teractions
can serveas an
pollinators.The timingof flowering
isolatingmechanismin plant speciation,whilethe
can limit
activity
timingof pollinatorand disperser
therangeof a plantspecies.In addition,thetiming
influencepopof seed productioncan profoundly
ulationdynamics.
Plant phenologyhas been moststudiedin the

141

142

Newstrom,Frankie,and Baker

inNewstrometal. 1993). CLASSIFICATIONS


BASEDON DATE.-Classification sysforanimals(see references
individ- temsderivedfromtemperate
Verylittleinformation
existsforlong-term
phenologyreferto the
surveys date or season of flowering
ual levelpatterns
becausethefewlong-term
(such as wet, dry,or
that have been conductedhave only superficially transition
season). Since the categoriesare usually
describedindividualpatterns(Koelmeyer 1959, based on data averagedover a numberof years
Medway1972, Dieterlen1978, CruzAlencar1979). ratherthanon a timeseriespattern,themain limOur data on long-term(12 yr) leafing,flow- itationof thissystemlies in theimpliedassumption
ering,and fruiting
cyclesin 254 treesfrom173 thattheflowering
patternhas an annualcycle.Our
speciesin thelowlandtropicalrainforestat theLa long-term
data showthattemporalsequencesin the
Selva BiologicalStationin Costa Rica have shown wet tropicsare oftennot annual, althoughmany
fourbasicpatternsat theindividualleveland gen- biologistshave a subjectiveimpression
thatpatterns
of pheno- have annual frequencydue to annual amplitude
eratednew insightsforthe organization
logical patternsat otherlevelsof analysissuch as peaks. Amplitudeis definedas the quantityor inWe focused tensityof response,for example, the numberof
thepopulation,guild,and community.
firston flowering
cycles,findingthemto be more flowerson a treeor the numberof treesflowering
and complexthan in any other in a population.Categoriesbased on date oftendo
diverse,irregular,
inan "on"/
annualflowering
patterns
ecosystem.This presentedproblemsfordescribing notdistinguish
patternsand led to thedevelopmentof a new clas- "off' cyclefrompatternshavingan annualampliapproach.In tude peak in a backgroundof lesserflowering
sification
allowinga morequantitative
all
this paper, we reviewthe limitationsof previous yearlong. Furthermore,
systemsbased on date of
of terms
fortropicalflowering
tendto promotea proliferation
patterns,then flowering
classifications
presentour classification
along withtheconceptual in the wet tropicswhereseasons are oftennot as
with highlydifferentiated
itsutility
framework
forusingit. We illustrate
as theyare in the temperate
examplesfromindividual,population,guild, and zone. Forexample,Croat(1978) had 26 categories
levelsof analysis.
of flowering
forthe tropicalmoistforeston Barro
community
Colorado Island in Panama.

PREVIOUS CLASSIFICATIONS
Severalclassifications
havebeenproposedtodescribe
that intropicalflowering
patterns.Classifications
criteriaare not
corporateadditionalnonflowering
discussedhere,suchas thosewithleafing(Reich &
Borchert1984) or with life form(Sarmiento&
Monasterio1983). There are threemain classificationsbasedon flowering
alone.The most
patterns
based on date or season,
widelyused classification,
phenology
(Croat
has beenimported
fromtemperate
1975, 1978; Tomlinson1980). Temperate-based
break down when
concepts,however,frequently
of tropicalplantsas has been
applied to characters
thecase withbranching
patterns
(Tomlinson& Gill
1973) and deciduousness(Richards 1952, Longofflowman & Jenik1987). The onlyclassification
forthe tropics
eringphenologydevisedspecifically
is thatof Gentry(1974). This has been the most
satisfactory
to date of thoseavailableand has been
used fairlywidely(e.g., Morellatoand Leitao-Filho
1990, Oliviera et atl. 1991). The strikingshortin thewetand drytropics
liveddisplaysofflowering
based on duinspiredanothertypeof classification
ration.This has been used in discussionsof pollinatorforagingbehaviorand reproductive
biology
(e.g., Frankieet ail. 1974, Augspurger1980, Bawa
1983).

GENTRY'S CLASSIFICATION.-Gentry(1974) created

a classification
to describetypesof floweringfor
The
Bignoniaceaein relationto pollinationsystems.
fivemajor classes,(big bang, multiplebang, cornucopia, steadystate,and an unnamedpattern),
a mixtureofcriteria
suchas individual
incorporated
levelamplitude,date,duration,and populationlevel synchrony.
temAlthoughthissystemidentifies
poral sequences well, it does not encompass the
range of diversityfound in our data. The classes
have been used impreciselyin the literaturebecause
some authors have used them for patterns that do

not meet all of the criteriaoriginallyspecifiedby


ofsome
theoriginaldefinitions
Gentry.Furthermore,
patternsinclude both individualand population
not
level criteriabut phenologistshave frequently
specifiedthese levels of analysis and oftenhave data

fromonlyone levelbut not both.

BASEDON DURATION.-Systemsbased
CLASSIFICATIONS

on durationdistinguish
betweenextremesof short
and long durationof flowering,
e.g., "seasonal" vs.
"extended" (Frankie et al. 1974), "mass" vs.
"steady state" (Augspurger 1983), and "mass" vs.
"extended" (Bawa 1983). As with categoriesbased

on date, such classes do not reveal the temporal


sequenceand lackexplicittimeand amplitudescales.

Plant Phenology

A major problemwith this systemis that some


termsreferto manydifferent
typesof patterns.For
example,"mass" has been used not onlyforfloweringthatlastsfora fewdaysorweeks(Augspurger
1980, Appanah& Chan 1981), but also formany
weeksor months(Perry& Starrett1980, Appanah
1982). It has referred
to patternsat a numberof
different
frequencies
(fromseveraltimesa yearto
multiyearcycles)and to many different
levels of
analysis(such as individual,population,and community).For example,"mass" (and relatedterms
such as "general"and "gregarious"flowering)
has
referred
to highamplitudeflowering
withmultiyear
cyclesthatare synchronized
amongmanyspeciesat
thecommunity
level(Janzen1978, Silvertown
1980,
Ashton1988).

143

of thesegraphs,the readermust not onlyextract


the natureof a givenpatternfroma complicated
overlayof severalpatterns,but also spend considerable time and memoryencodingand decoding
numeroussymbols.Cleveland (1985, p. 25) resolvedthisproblemforothertypesof data by juxtaposingtheeventsalong thesame timeaxis using
thesame symbols.Followingtheseand otherprinciples of graphicsin Cleveland (1985), we have
developednew typesof graphicaldisplaysto produce greatervisual clarityfor tropicalphenology
patterns.

THAT ARE NOT COMPARABLE-One


of the
main problemsimpedinga synthetic
treatment
of
in comparing
tropicalphenologyhas been difficulty
resultsamongstudiesdue to a lack of standardization in termsand methods(Frankieet al. 1974,
Bawa & Hadley 1990). There are severalreasons
PROBLEMS IN TROPICAL
whytropicalphenologytermsareoftenambiguous.
PHENOLOGY
In manycases, the same termhas been used for
PATrERNS THAT ARE NOT REVEALED.-Because
phenomena(such as "mass" or
cycles severaldifferent
themain problemin "steadystate"),or thesame phenomenonhas been
are so complexand irregular,
Thus the measuredwithmanydifferent
methods,or different
tropicalphenologyis patternrecognition.
role of graphicsand choice of graphicalstylehas time or amplitudescales. Conversely,a profusion
criticalimportance.
Numericalsummarieshave of- of different
termsmay referto the same pattern.
in our classifiten obscuredtemporalsequencesin tropicalphe- For instance,subannual flowering
nology(e.g., reportsof 5 mo reproductive
cyclesin cationhas been referedto as "episodic" (Bullock
figs(Koelmeyer1959) and 7 to 10 mo cyclesin et al. 1983), "periodic"(Haber & Frankie1989),
Delonix regiaand Lagerstroemia
speciosa(Richards "intermittent"
(Koelmeyer1959, Medway 1972,
1952) lack a measureof varianceand therefore
do Berg 1989) and "multiplebang" (Gentry1974).
in cyclelengths).Ex- In our classification,
we have therefore
used consisnot readilyrevealirregularity
Data Analysis(Tukey 1977) and thein- tentand precisely
definedcriteria,
exploratory
incorporated
the
creasingpower of computersand softwarehave plicittimeand amplitudescales,and restricted
spawnedthe fieldof graphicalanalysis(Cleveland numberof termsemployed(see glossaryin Appen1985). Graphicscanrevealunexpected
relationships dix and discussionin Newstromet al. 1993).
because theydisplaylargeamountsof information
of points PATTERNS THAT ARE CONFUSED AT DIFFERENT LEVwhile retainingthe relativearrangement
in a way thatnumericalsummariescannot(Tufte ELS.-Part of the complexity
of tropicalphenology
in patternsfromone level
1983, Cleveland 1985, Pickover1990). By using is due to the differences
graphs ratherthan numericalsummariesin phe- of analysisto another(see Table 1). Althoughsevbetweenindividualand
nology,formerly
obscureflowering
patternscan be eral authorsdistinguished
revealed(see below). Our searchfornew pheno- populationlevels (e.g., Augspurger1980, 1981;
logical patternshas been expeditedby rapid gen- Piiieroand Sarukhan1982; Bullock et al. 1983),
erationof thousandsof computergraphs,an im- phenologistshave not systematically
incorporated
levelsof analysisintothelanguageof tropicalphepossibletask by hand.
The choiceof graphicalstylemay obstructor nology.This is due to thecommonassumptionthat
In tropicalphenology,tra- patterns
arethesameat all levelsfora givenspecies,
aid patternrecognition.
ditionalgraphshaveservedas visualobstaclecourses whichis oftentruefortemperatephenologywhere
whenever- wintersynchronizes
mostspeciesintoannualcycles
morethanas toolsforpatternrecognition
they superimposemultiple events (e.g., leafing, at all levels. However,it is not true for tropical
and fruiting)along the same time axis phenologywherepatternsmay differat different
flowering,
in the examplesbeusingeitherlineplotsor a varietyof different
sym- levelsof analysisas illustrated
bols (e.g.,Medway1972). To perceivethemeaning low.
PATTERNS

144

Newstrom,Frankie,and Baker

METHODS
Data collectionproceduresforthisprojectand site
forthe La Selva BiologicalStationin
information
Costa Rica have been describedin Frankieet ail.
(1974) and Newstromet ail. (1993). Using binoculars,monitorsmade monthlyobservationsof
on 457
and fruiting
leafing,budding,flowering,
tagged treesfromJanuary1969 to March 1981.
Only thosetreeswitha minimumof 5 consecutive
wereused fortheclassification,
yearsofobservations
173
in a sampleof 254 treesrepresenting
resulting
speciesin 59 families.In this sample, 11 species
by 4 to 6 trees,78 speciesby 2
wererepresented
by one tree.The amor 3 treesand theremainder
plitudescalehad threeclasses:none,light,and heavy
withrespectto thetypicalcropof flowers
flowering
foreach tree.Wherevertherewere threeor four
treesavailable fora givenspeciesin our data, we
estimateda populationlevelpatternby calculating
of treesin flowerat each intervalin
theproportion
the timeseries.Seasonsat La Selva have been classifiedas main dry fromJanuaryto May; early
wet fromMay to September;veranillo, an unpredictabledryseason, in Septemberor October;
and, late wet fromOctobertoJanuary(Newstrom
et ail. 1993).
patternsforma continBASIC CLASSIFICATION.-The
flowering.
uum fromcontinuousto veryinfrequent
fourbasic classesbased on freWe distinguished
quency,definedas thenumberof"on'"/"off"cycles
episode
per year(one cycleconsistsof a flowering
interval,Fig. 1). The
followedby a nonflowering
four basic classes are continual (floweringwith
sporadicbriefbreaks), subannual (floweringin
more than one cycleper year),annual (only one
majorcycleperyear),and supra-annual (one cycle
overmorethanoneyear)(Figs.1 and 2). Regularity,
is
as a secondarycriterion,
used in theclassification
epidefinedas the variancein lengthof flowering
intervals,
and consequently
sodes and nonflowering
ofthecyclesas well(Fig. 1). We initially
recognized
two main classes, regularand irregular,but are
in moredetail.
thiscriterion
quantifying
presently
suchas duThe classification
uses othercriteria
subdividethe
ration,amplitude,and dateto further
classes(see Newstromet al. 1993). For example,
we divideannual flowering
patternsintothreeduflow(< 1 mo), intermediate
rations:briefflowering
(>5 mo).
ering(1-5 mo), and extendedflowering
We base othersubcategorieson the shape of the
curveforamplitudeof flowering
(see Fig. 11.8 in
Newstromet ail. 1993). Furthersubdivisionsare
as themonthor season.
based on date,represented

00

00

00

ON
ON

0
4.4
60

00

ON

ON
-4

-.,

tc

0 00

r-

r-

00

CZ

44
CZ

-a

00
C) ." ON
0
0
CZZ
,

oo

00

00

ON
-4

tu

44

ol
0

CZ
0

7:1

-0 C:

Plant Phenology

CLASSES

FREQUENCY

Continual

145

24

12

24

36

48

60

72

84

96

108

120

132

Sub-annual
24-

12

24

36

48

60

72

84

96

108

120

132

12

24

36

48

60

72

84

96

108

120

132

1;

1;.

1,

96

108

120

132

04.

*3

Annual

'].

11;

12

0
?

11,

---,--

---.

24

36

,;11

48

60

72

84

0 .. . . . . . . .. . 0.... .. . .. ; . . . . . . .. . ... . . . I....... ... I. . . . . I. . . . . ... . . . I... ...... . 11..; .. ..

2S~upra-annual

01
12

24

36

21

24

60

72

84

96

108

120

132

108

120

132

REGULARITYCLASSES

Regularpattern

12

48

36

48

60

72

84

96

Irregular
pattern
21
.. .. .

12

24

.. .. ..

36

. ; ..

48

. . . .;..

60

72

. .

.. ..

..

.. . . . . .

84

96

. ..

108

.. . .

120

132

Time: 144 months


classesand two regularity
classeswithamplitudeheld constantto
FIGURE 1. Idealized diagramof fourfrequency
revealthe essenceof each criterion.

146

Newstrom,Frankie,and Baker

Guatteriaaeruginosa

Continual

Tree 1043

1-llllllll l
ll lll
ll
HliiiHliiiltiii iiiii iii11111iilillilt,lll
ii
,

12

24

36

48

60

72

84

96

120

108

132

a)

Sub-annual
o0
2
r_: 0

-~

Protiumpittieri

.. .....
,

.......... 1...

~~~~~~~8

18

~Lonchocarpusoliganthus

I2

I.
12

t .......IlI.,II - .11111!l
.1111.,....1.1l!ll l11 1II1II ! 11 .
60

Annual

Tree 1102

24

36

48

60

I,
72

Tree 1004

11111

84

96

120

108

Sapranthuscampechianus

Supra-annual

132

Tree 2173

2-

.... .....

I
12

24

36

I........ ......I .......1..1..


.........
48

60

72

84

96

108

120

- . - .1
132

Timeinmonths:Jan1969 - Dec 1980


FIGURE 2. Time seriesgraphsshowingthe frequency
in fourbasic flowering
and regularity
patterns(S program
high densityplot in Beckeret al. 1988). Each graphshows monthlyflowering
from1969 to 1980 forone treeof
each of fourspeciesin the lowlandtropicalrain forestat the La Selva BiologicalStation.Amplitudecategoriesare:
I = lightflowering,
2 = heavyflowering,
dots on the x axis = no flowering,
blanks= missingdata.

We reservethe termseasonalityto mean the temwitha certainmonth


poral associationof flowering
or seasonof theyearand not to referto an annual
frequency
as is commonlydone in phenologylitpaterature.Thus, anyof thefourbasic frequency
ternscan have seasonal associationsrelatedto the
most oftenoccursor when
dates when flowering
is heaviest.
flowering
THE INDIVIDUAL LEVEL.-Three

differentgraphical

the fourbasic patterns:


presentations
characterize
timeseriesgraphs(highdensityplotsin S program,
and regBeckeret al. 1988) show the frequency
ularityof cycles(Fig. 2), matrixgraphsshow the
durationand date (Fig. 3, lower half), and bar
frequency
graphsportrayseasonalityof flowering
and amplitude(Fig. 3, upper half).
In the continualpattern,shownin Guatteria
aeruginosa(Annonaceae),flowerproductionceases

onlysporadically
and briefly
(Figs. 2 and 3). Continualpatterns
haveseasonaltrendsforhigherprobabilityof heavyflowering
(e.g., in bothdryseasons
in Guatteriaaeruginosa(Fig. 3, upper half) and
both wet seasonsin Hamelia patens(see Fig. 11.7
in Newstromet al. 1993)).
The subannual flowering
patternis the most
irregularand poorlyunderstood.The pattern,as
shownin Protium
pittieri(Burseraceae),has several
unpredictable
flowering
cyclesperyear(Figs. 2 and
3). Althougha few yearshave only one cycleof
flowering,
mostyearshave several.This illustrates
of long timeseries(at least 5 yr)to
theimportance
fullydescribepatternsin tropicalphenology,althoughsome patternsmay be inferred
fromshort
termpopulationstudies.Three distinctive
features
this pattern:flowering
characterize
episodes occur
at anytimeof theyear,bothflowering
episodesand
nonflowering
intervals
varygreatlyin duration,and

Plant Phenology
CONTINUAL

Protium
pittieri

Lonchocarpus
oliganthus

Sapranthus
campechianus

Tree 1102

Tree 1004

Tree2173

JFMAMJ
JASOND

JFMAMJ
JASOND

JASOND
JFMAMJ

Tree 1043

1.0

SUPRA-ANNUAL

111111.I.
'11i111
Guatteria
aeruginosa

CIO

ANNUAL

SUB-ANNUAL

147

0.5
0.0-

JFMAMJJASOND

69
70
71
81
72
73
74
t8 75
>-4 76
77

.00.
.0000000000.so**.*.....
@001
----00----

78

00
*

@ 00
00.-

000

*0*

79
80

JFMAMJJASOND

000

0.

0.0

**0

000@
0 000000
00.000
@000O000

@0
@0

@0

0000

@0000
@

0
JFMAMJJASOND

JFMAMJJASOND

JFMAMJJASOND

Month
FIGURE 3. (a) Upper panel: Bar graphsshowingseasonalityin fourbasic flowering
patternsas proportionof years
forone treefrom
in whichheavyor lightflowering
occurredforeach monthof theyear.Each graphshowsflowering
1969 to 1980 fromeach of fourspeciesin the lowlandtropicalrain forestat the La Selva BiologicalStation.Light
dark shading = heavyflowering.(b) Lower panel: Matrixgraphs(yr by mo) showing
shading = lightflowering,
durationand date in fourbasic flowering
patterns.Each graphshowsone treeforthe same speciesas the seasonality
blanks= no flowering,
lightshaded circles= lightflowering,
bargraphsabove. Dark shaded circles= heavyflowering,
dots = missingdata.

consequentlythe numberof cyclesper yearvaries


as well. These patternshave seasonal associations
occursmostoftenand when
forbothwhenflowering
flowering
is heaviest.In thecase of P. pittieri,most
flowering
occursin theearlywet seasonat La Selva
but in otherspecies,such as Guarea rhopalocarpa
sprucei(Myristicaceae)
(Meliaceae) and Compsoneura
mostflowering
occursin both dryseasons(see Fig.
11.7 in Newstromet al. 1993).
Annual flowering
has onlyone majorflowering
in Lonchocarpus
oliepisodeper year,as illustrated
ganthus(Fabaceae) (Figs. 2 and 3). This patternis
the most regularone and has the most consistent
durationsforboth the flowering
episodesand the
This patternusuallyhas manonflowering
intervals.
jor flowering
episodes that are constrainedto one

time of the year.Variationsof the annual pattern


includethe pulsed annual patternwithpauses emepisode as foundin
bedded in the majorflowering
Vellozia squamata (Velloziaceae) in the cerradoof
neotropicalBrazil (Oliveira et al. 1991) and in
(Violaceae) in temperateNew
Melicytusramiflorus
with
Zealand (Powleslandetal. 1985); and patterns
additionallow amplitudeprecociousor tardybrief
that sporadicallyoccuroutside
burstsof flowering
episode(see Fig. 11.8 in Newsthemain flowering
tromet al. 1993).
shown in Sapranthus
Supra-annualflowering,
episodes
(Annonaceae)has flowering
campechianus
in multiyearcycles(Figs. 2 and 3). Some supra(one or two in
annual patternshave rareflowering
"alternate"
12 yrs)but othershave approximately

Newstrom,Frankie,and Baker

148

Lonchocarpusoliganthus
Tree1003

Annual

12

2
2~

24

36

48

60

72

84

96

108

120

Tree 1004

Annual

12

24

36

48

60

84

72

96

108

120

132

Annual

144

Tree1196

..........

12

144

132

24

1 .......I

36

48

.. ..

. 11 .

60

. 11

72

11 1 .

84

96

108

120

144

132

Proportionofall threetreesin flower


ll

1.0 1

00.

......

12

.. . .

24

.. . . .

36

. . . .

48

.. . .

60

l
. . . .

72

.. . . .

84

. . . .

96

.. .. .

108

III

.. . . .

120

. .

132

. .

.
144

Time in months: Jan1969 - Mar 1981


FIGURE 4. Estimateof possible annual patternat the populationlevel based on threeannual flowering
patterns
in individualLonchocarpus
trees.The top threepanelseach represent
a timeseriesforone tree.The bottom
oliganthus
thesum of the threeindividualpatternscalculatedas theproportionof treesflowering
panel represents
in each month
of each year.More than threetreesare needed fora betterestimateof populationpatterns.

flowering
everytwo to severalyearsThese patterns
have too fewdata to determinethe regularity,
duration,or seasonalityof flowering
and will not be
discussedfurtherin this paper (see discussionin
Newstromet al. 1993).

THE CONCEPTUAL
FRAMEWORK

plied to anylevelof analysis.Profilesof therelative


abundanceof patternscomprisingeach level demonstratethe diversityof patternsin tropicalphenology(see communityhistogrambelow). Unlike
temperatespecies,tropicalspeciescommonlyhave
heterogeneouspatternsat a given level. For example,a populationmaybe composedofindividual
patternsthatdiffer
becauseofage and size (Borchert
1978), gender(see Fig. 6 forCompsoneura
sprucei
and Fig. 11.6 in Newstromet al. 1993), or miIn addition,patternscan difcrohabitatdifferences.
ferfromone levelof analysisto thenext,especially
in tropicalphenology(Table 1).

We separatedpatternsat each level of analysisso


thatadding the timeseriesat each timeintervalat
one levelproducesa timeseriespatternforthenext
higherlevel (Table 1, Figs. 4 to 6). Levels are
hierarchically
arranged:flower,
inflorescence,
branch,
the populationlevel,
branchcomplexes,individual,populationand com- THE POPULATION LEVEL.-At
patternmaybe simpleand composed
munitywith additionalnon-nestedlevels such as theflowering
the guild. The fourbasic frequency
classesare ap- of only one type of individualpattern,or mixed

Plant Phenology

149

Guarea rhopalocarpa
Sub - annual
ot

1III.

11.111

12

Male tree1020

24

.1,11

36

ll

.,

l .

48

,11

60

1,1

72

1 1 ,1

84

1I

108

96

Sub - annual
t:

12

24

36

48

60

72

1111,1,1~
84

11

~~~~~~~1

108

96

12

...
.. . .

..........
24

144

.;_

1.111
120

132

144

Femaletree1149

Sub - annual

0.H.....

132

Femaletree1048

I 111111 1 11l 11 11lll 11 11ll

oq

d~~~~~~~~~~~~~~

120

36

48

60

72

84

96

... ......
108

120

..
132

144

Proportionofall threetreesin flower

-f

1.0

os~~~~~~~~~
12

24

|
36

||
48

||
60

72

1|||1111
84

96

108

1 11 1110ll1l.I1 1111
120

132

144

Time in months:Jan 1969 - Mar 1981


patternat the populationlevel based on foursub-annual
FIGURE 5. Estimateof possible subannual flowering
ofgraphsame as in Figure4. The subannual
trees.Arrangement
flowering
patternsin individualGuarea rhopalocarpa
by data from119 treesin Bullocket al. (1983).
populationpatternforthisspeciesat La Selva is confirmed

and composed of more than one type.The organizationof individuallevelpatternsintopopulation


forcontinualand
level patternsis straightforward
but not forsubannual(Table 1).
annual flowering
a continualindividualpatA populationcontaining
ternalwayshas a continualpopulationpattern.Similarly,a population with only annual individual
patternsalwayshas (as faras we know) an annual
populationpatternas in Dipteryxpanamensis(Perry
& Starrett1980, Newstromet al. 1993) and posoliganthus(as suggestedby
sibly in Lonchocarpus
the threetreesin our data in Fig. 4).
In a populationwithonlysubannualindividual
patterns,however,the populationpatternwill be
eithercontinualor subannual dependingon the
among
numberoftreesand thedegreeofsynchrony
individualsof Guarea
trees.Subannuallyflowering

rhopalocarpa
(Fig. 5), a dioeciousunderstory
treeat
La Selva, appearto have sufficient
populationlevel
synchrony
to producea subannualpopulationpatternwith 119 trees (Bullock et al. 1983). The
in thiscase,occursmorein thenonflowsynchrony,
eringintervalsthanin the flowering
episodes,suggestingthat conditionsinhibitingfloweringmay
governthe pattern(see Newstromet al. 1993 for
further
discussion).In contrast,moreasynchronous
populationswould producea morenearlycontinual
pattern,such as we have estimatedfromfourtrees
of Compsoneura
sprucei,an understory
dioecioustree
at La Selva (Fig. 6). In thisspecies,two typesof
individualpatterns,subannualand annual,appear
to be correlated
withgender(see Bullock 1982 and
Newstromet al. 1993), althoughmore data are
needed to confirmthis.The genderdifference
fol-

150

Newstrom,Frankie,and Baker

Compsoneurasprucei
Sub - annual

Male tree1009

2-

12

24

36

48

60

72

84

96

108

Sub - annual

120

132

144

Male tree1141

2-

1 I
i

11, I
12

. .. . . I... I . . ...1 .. ..I..1 . I1 111 .1 l


I. I..........1 .. 1 1.... ....1IJ I11 11l

I 111
.1
24

36

48

60

72

96

84

108

HI 11111
I IIIII I

,C
.4

132

144

Femaletree1118

Sub- annual
21-

120

I11,11

1I

I! 1III

H0-11.11.1l

0
12

24

36

48

60

72

84

96

108

120

132

144

Annual

Femaletree2054
. . . . . . I . . . . . . I . .... . . . . . I . . I

o . . .. ..
12

24

36

48

60

72

84

. . . . . . . . . . . . . . . .I. . . . . . I. . . . . . .
96

108

120

132

144

120

132

144

Proportionofall fourtreesin flower

1.0 3.5

12

24

36

48

60

72

84

96

108

Time in months: Jan 1969 - Mar 1981


FIGURE 6. Estimateof a possiblepopulationpatternapproachinga continualpatternbased on threesubannual
of graphsame as in Figure
patternsin individualCornpsoneurasprucei trees.Arrangement
and one annual flowering
4. More than fourtreesare needed fora good estimateof thispopulationpattern.There appearsto be a trendfor
of this
males to have subannualindividualpatternsand femalesto have annualindividualpatterns,but confirmation
requiresa largersample of treesthan in our data and a longertime seriesthan in Bullock (1982).

lows the trendshown in many otherspecieswith THE GUILD LEVEL.-Guild


level patternshave four
male plantsflowering
morefrequently
The presenceof gaps (or
thanfemales importantcharacteristics.
(Lloyd& Webb 1977, Bawa 1983, Clark& Clark nonflowering
sequence
intervals)in themultispecies
1987). Selectionforsubannuallyflowering
treesto affects
of thepollinatorpopulation
themaintenance
forma strictly
continuouspopulationpatternoccurs throughout
theyear.Continualguild patternshave
in figs,wherelocal survivalof fig-wasppollinators no gaps and annual guild patternshave significant
dependson theconstantavailabilityofreproductive gaps duringwhichpollinatorsare dormantor abtrees(Newstromet al. 1993). A reinterpretation
of sent.The amountof overlapamong speciesaffects
figphenologyusingour classification
is beingpre- the degreeof interspecific
pollen mixingand may
sentedelsewhere.
be relatedto competitionforpollinators(Rathcke

Plant Phenology

151

1983, Rathcke & Lacey 1985, Pleasants 1990, annual(Fig. 8). This mixedsequencehad no gaps,
Newstromet al. 1993). Changesin amplitudeof extensiveoverlap,and a strongunimodalseasonal
by Stiles(1978)
affectthe numbersand level of activity peak. This examplewas illustrated
flowering
of the pollinators(Bawa 1983, Rathcke& Lacey as an averageforthe fouryearsratherthana time
ofthespeciesmay series,butpresumably
1985). Finally,thepermutations
theorderofspeciesflowering
be retainedin the same orderfromyearto yearif eachyearchangesbecauseoftheinherent
irregularity
cued, as of subannualpatterns.The mixedpatternhas not
each speciesis stronglyand differentially
with markedregular beenwell-studied
is commonin environments
but itprobablydominatesin polfivetypesof pollinator linatorguildsoflowlandtropicalrainforest
seasons.We have identified
because
(Table 1).
guild patternsusingour classification
of the prevalenceof subannualflowering
patterns
patternat the (Newstromet al. 1993). The staggeredsequence
The staggeredannual flowering
guild level is one of the mostfamiliarbecauseit is maydominatein moreseasonalecosystems
suchas
so commonin the temperatezone. In the tropics, temperate
and tropicaldryforests.
The effects
of an
it occursin both wet and dryforests.The pattern overlappingmixedmultispecies
sequencewithunof annual populationpat- predictablespeciespermutations
comprisesa progression
on pollinatorspeternsin a sequenceof speciesthatextendsforonly cializationand foragingpatternshave not been inpart of the year.For example,in lowlandtropical vestigated.
rainforest
at La Selvabeetlepollinatedspeciesflower
Some mixedcontinualflowering
patternsat the
in a staggeredsequenceforpartof theyear(Young guildlevelhavedramaticamplitudepeaksat supraintervalor annualfrequencies.
1986, 1990). Duringthe nonflowering
This guildpatternhas beendegap the beetlesare dormant.In the tropicaldry scribedforthrippollinatedspeciesin Malaysia(Chan
forestin Guanacaste,Centrisand otherlarge bee & Appanah 1980; Appanah & Chan 1981; Appollinatedspeciesflowerin a staggeredsequence panah 1985, 1990; Yap & Chan 1990; La Frankie
offlowering & Chan 1991). Aftermanyyearsof sporadiclight
duringthedryseasonwhena profusion
a staggeredbut slightlyoverlappingseoccurson leaflesstrees(Frankieetal. 1976, 1983). flowering,
The bees are in diapauseduringthegap in thewet quence (Ashtonet al. 1988) of six Shoreaspecies
At thistime,
season.Whetheror not thesepatternshave signif- burstintofull,highintensity
flowering.
tested.The theshort-lived
icantoverlaphas not been statistically
thrippollinators
havean exponential
of speciesare similareach year.
permutations
populationexplosion.At othertimes,otherspecies
The staggered
continualflowering
patternat the thatflowermorefrequently
at low or intermediate
guildleveloccursinhermit
pollinated amplitudesmaintainthe thripsat low population
hummingbird
speciesat La Selva (Stiles1978). This patterncom- levels.
prisesa yearlongcontinualsequenceof 10 different
A specializedcontinualflowering
patternat the
specieswith annual populationpatterns(Fig. 7). guild level in figspeciescomprisesbothsubannual
Only one minorgap occurredin 1973 in thisex- and supra-annualindividualpatternsat the indiample whenCostusruber(species5) did notflower. vidual level(Miltonet al. 1982, Michaloud 1988,
These speciesdid not overlapsignificantly
(Stiles Windsoret al. 1989). In thiscase the guild level
1979, 1985; Cole 1981; Pleasants1990 and see is equivalentto the populationlevel because the
discussionin Newstromet al. 1993). Yearly bi- pollinationsystemis speciesspecific.The continual
modal peaks in amplitudeof flowering(Fig. 7, patternat the guild level is essentialforfig-wasp
withhermithumming- survivaland thesubannualpatternat theindividual
lowerpanel) are correlated
bird breedingand moultingtimes (Stiles 1975, level may be selectedbecause it enhancesthe pol1977, 1978, 1980, 1985). The orderof permu- linatorattractant
and promotesoutcrossing
(Janzen
tationsof specieswas similareach yearwithonly 1979, Bronstein1989, Frank 1989, Bronsteinet
minorvariations(Fig. 7).
al. 1990, Newstromet al. 1993).
The mixed continualflowering
patternat the
guild level withannual cyclesof amplitudepeaks THE COMMUNITY LEVEL.-Although the community
withthestaggered
contrasts
continualpatternmain- level pattern has been examined for a number of
ly because of the extensiveoverlapand the disor- lowlandtropicalrainforests
(e.g.,Koelmeyer1959,
dered permutationof species each year. For ex- Medway 1972, Dieterlen1978, CruzAlencaretal.
ample,27 speciesofplantspollinatedbynonhermit 1979, Putz 1979, Van Schaik 1986) the rangeof
hummingbirds
at La Selva (Stiles 1978), consistof diversity
in populationand individualpatternshas
flow- not been well described.The profileof individual
overlappingpopulationswithmanydifferent
eringpatternsincludingcontinual,subannual,and patterns,
calculatedas therelativeabundanceofeach

Newstrom,Frankie,and Baker

152
1

*6000

060

*660

e00

060

060

060

006600000

06

106

as

6S

66

0 6

a@

60

10

66

@6

060

00600

060

0 6

JFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASOND

0.6
C)

0.4-

C
C
o

0.2-

0.

J FMAMJ

J AS ONDJ

FMAMJ

J AS ONDJ

FMAMJ

J ASONDJ

FMAMJ

J AS OND

Timein months:Jan1971 - Dec 1974


patternat the guild level in hermithummingbirdfood plants from
FIGURE 7. Staggeredcontinualflowering
January1971 to March 1975 in the lowlandtropicalrainforestat the La Selva BiologicalStation.The populations
of 10 speciesfloweredwithonlyone briefbreak,in almostthe same permutationeach year,and withno significant
overlapamong species.Species are: 1 = Heliconiapogonantha,2 = Passifloravitifolia,3 = Heliconiawagneriana,4
= Justiciaaurea, 5 = Cpstusrtiber,
8 = Aphelandrastorkii,9 =
6 = Heliconiairrasa, 7 = Heliconiaumbrophila,
(Adapted fromFigure5 in Stiles 1978.)
Heliconiamathiasiu.,10 = Costusmalortieanus.

typeof flowering
patternforLa Selva, shows that
moretreeshad subannual(55%) and annual(29%)
flowering
patternsthancontinual(7%) and supraannual (9%) ones (Fig. 9). Within the treecommunityat La Selva, canopyand subcanopystrata
have different
profiles(Newstrom et al. 1991).
Differenttypesof tropicalrain forestsmay have
different
profilesin relationto changesin rainfall

distribution
or floristic
composition.For example,
supra-annualflowering
patternsmay dominatein
dipterocarpforestsof Malaysia. Major ecosystems
in phenologicalprofiles.For
show largedifferences
instance,temperateforestshave annualcommunity
patternswithspecieshavingtwo main population
patterns(annual and supra-annual)in contrastto
lowland tropicalrain foreststhat have continual

Plant Phenology

-a

Af

Aft8

all
communitypatternswith species representing
fourtypesof populationpatterns.

sS,-

3~~~~
61
717
8
10

19

15
21
16
122
17
23
18*24
19
20

21

22
23
24
26
27

!!=
J F MAM

0.6

J J A S ON D

00

*~

*_14

0.2-

0.0
J FMAMJ

153

J AS OND

Time: One yearin months

GEOGRAPHIC VARIATION IN PHENOLOGICAL


PATrERNS.-Tropicalspecies oftenhave flowering
in different
ecosyspatternsthatdiffer
dramatically
tems, consequentlywe cannot always describea
pattropicalspeciesas havinga "typical"flowering
tern(Borchert1980, 1986; Huxley 1983; Akunda
& Huxley 1990). The geographicvariationin phenologicalpatternswithinthe same speciesis more
noticeablein the tropicsthan the temperatezone
because phenologicaldiversityis higher.In some
species,the flowering
patternsare invariantover a
wide range of environmental
conditions.For example, Cedrelaodorata,Cordiaalliodora,and Castilla elasticaall havethesame annualseasonalcycle
in thelowlandtropicalrainforestat La Selva (Frankie et al. 1974), the tropicalmoistforestat Barro
Colorado Island in Panama (Croat 1978), and the
tropicaldry forestat Guanacaste in Costa Rica
in(Frankieet al. 1974). Possible environmental
fluenceson flowering
thatare in commonin these
havenotbeenexploredforthese
different
ecosystems
species.
In otherspecies,patternschange dramatically
fromone ecosystem
to another.Some specieschange
in thewettropics
to a higherfrequency
of flowering
thanin thedrytropics.Forexample,in thelowland
tropicalrainforest,treesof Hamelia patensflower

patternat the
FIGURE 8. Mixed continualflowering
guild level in nonhermithummingbirdfood plants averaged over 4 yrs from 1971 to 1975 in the lowland
tropicalrainforestat the La Selva BiologicalStation.The
guild patterncomprisescontinualfloweringin species
in speciesnumber
number1 and 2, subannualflowering
in speciesnumber7 to 27.
3 to 6, and annual flowering
The populationsof 27 speciesfloweredwithno gaps and
extensiveoverlap.The permutationspresumablychange
timein
each yearbecause of the unpredictableflowering
subannualpatterns.Speciesare: I = Cephaelistomentosa,
2 = Hamelia patens, 3 = Symzphonia
glohulifera,4 =
Colurmnea
5 = Colusmnea
linearis,6 = Vrienicaraguensis,
sea gladioliflora,7 = Aechmeamexicana,8 = S-hlegelia
sp., 9 = Aechmeamaria-reginae.10 = Gesneriac-eaesp.,
11 = Gurania levyana, 12 = Gurania c-ostaricensis,
13
= Odontonema
14 = Aechmeanudi-aulis,15 =
tubiforme,
Renealmiaexalta, 16 = Heliconiamariae,17 = Erythrina
cochleata,18 = Cephaeliselata, 19 = Heliconialatispatha.
20 = Besleriasp., 21 = Renealmiacernua,22 = Guzm,ania
23 = Warscewicziacoccinea,24 = Heli-onia
monostachia,
imbricata,25 = Heliconiasarapiquensis,26 = Alloplectus
coriaceus,27 = Razisea spicata. (Adapted fromFigure4
in Stiles 1978.)

154

Newstrom,Frankie,and Baker

in a continualpatternwithlightestflowering
in the
dryseasons,while in the tropicaldry forest,trees
of thisspeciesflowerin an annual patternwithno
in the dryseason (Frankieet al. 1974).
flowering
This patternshiftsuggeststhat lack of moisture
inhibitsflowering
in thisspecies.The influenceof
on flowering
patternshas been inhydroperiodicity
vestigatedinmanytropicaldryforest
species(Borchert 1980, 1983, 1991; Reich & Borchert1982,
1984) but has notbeen studiedin lowlandtropical
rainforestspecies.
The reversepatternshiftoccursin otherspecies.
These changeto a lowerfrequency
of flowering
in
thewettropicsthanin thedrytropics.Forexample,
in both Andira inermisand Ceiba pentandratrees
flowerlessfrequently,
in raresupra-annualpatterns,
inside the lowland tropicalrain forestand more
in alternate
frequently,
supra-annualpatterns,
in the
tropicaldryforestand along edges of the lowland
tropicalrainforest(see Newstromet al. 1993). In
Africa,C. pentandraflowered
regularly
in an annual
patternin the dry forestand in a supra-annual
patternin thewet forest(Baker 1965). Shoreaspecies in Malaysiademonstrate
a similarpatternwith
treesfloweringmost oftenand regularlyin drier
in wet forests,
forests,
supra-annually
and hardlyat
all in swamp forests(Yap & Chan 1990). This
suggeststwopossiblemechanisms:
a dryperiodmay
be requiredforfloralbud induction("xeroinduction, Bernieretal. 1981) orhigherlightconditions
may promotegreaterflowering
frequency.Experimentalevidencefor"xeroinduction'of flowersin
the lowland tropicalrain forestexistsforthe herbaceous Geophilarenaris(Bronchart1963, Bernier
et al. 1981) but thishas not been investigated
for
trees.
A change fromirregularsubannual flowering
patternto two regularcrops per yearwith introduction of droughthas been reportedfor Citrus
trees(Monselise& Goldschmidt1982) but, otherwise,reportsofchangesinvolvingsubannualfloweringarerarebecausethispatternhas notpreviously
been well recognized.

CONCLUSIONS
The effectiveness
of a classification
schemedepends
ofthecriteria
that
on severalfactors:theimportance
are givenpriority
fordelineatingcategories,
thedegreeofsimilarity
amongmembersin each category,
and the degreeof difference
amongcategories(i.e.,
The more consistent
frequencyof intermediates).
the associationsamong descriptorsfor categories,
If the charthe more successfulthe classification.

6050 -

40 z

30 g
0

20-

10

ContinualSub-annual Annual Supra-annual


FIGURE 9. Histogramof relativeabundanceof indiflowering
pattern
vidualpatternsmakingLp thecontinuLal
at the treecommunitylevel in the lowland tropicalrain
forestat La Selva BiologicalStation.The fourbasic pattrees.
ternsare representedas percentagesof individuLal
This is the appropriateuinit of analysis.The same data
calculatedas percentageof speciesratherthan treesgive
similarresults.Only treeswith - 5 yrof consecutivedata
patternsand
were included,and intermediateflowering
palms wereexcluded.

acteristics
are distributedrandomlyamong classes
or if classesintergradein a continuum,the classificationhas less usefulness.The most important
stricture
about classifications,
however,is thatthey
usedthattheylimitcreative
do notbecomeso rigidly
perceptionwhenevernew contextsare moreappropresent
priate(Bohm & Peat 1987). We therefore
as a convenient
thisclassification
wayto bringorder
to the complexityof phenologicalpatternsin the
wet tropicsand not as a replacementforprevious
classifications.
has
The main contribution
of thisclassification
in tropicalpatternsat
been to clarify
thedifferences
different
levelsof analysisand to providea logical
The resultsof our quansystemforquantification.
titativedescriptionforpatternsusing the variables
of frequency,
duration,amplitude,date,
regularity,
will be publishedelsewhere.Using
and synchrony,
frequency
of "on"/'off" cyclesbased on an annual
time scale as the criterionfordividingthe classes
ratherthan yearlyseasonal averagesportraystemforirregporal sequencesmoreclearly,particularly
ular subannualand supra-annualpatterns.The explicittimeand amplitudescalespermitstandardized
comparisonsamong studies. For example, differ-

Plant Phenology

155

phenologyin lowlandtropentiating"on''/off' cyclesfromothercyclesde- in describingflowering


finedaccordingto amplitudepeaks would clarify ical rainforesttrees.The classification
capturesthe
of phenologicalpatternssuch as the fullrangeof diversity
descriptions
and clearlyrevealsirregular
annual patternsreportedin fig species by Frank temporalsequencesthat are so common in this
thisfigpatternis de- ecosystem.Four basic patterns(continual,suban(1989). In our classification,
whichcom- nual, annual and supra-annual)are applied to describedas subannualindividualpatterns
bine to forma continualpopulationpatternhaving scriptions
of patternsat each level of analysisfrom
of the flowerto the individual,population,or comstrongannual amplitudepeaks. The simplicity
of
usingthe same fourbasic patternsat each level of munityas well as the guild. The quantification
oftropicalflowering patterns
one ofthemajor
analysisreducesthecomplexity
promotesstandardization,
of problemsin tropicalphenology.This systemsimproliferation
patternsand eliminatesa confusing
plifiesthecomplexity
and accentuatesthediversity
terms.
Each of the levelsof organizationhas its own of tropicalflowering
patterns,and therebyopens
of phenology.The individual theway to moremeaningful
and accuratecomparvalue fordescription
to theobvious isonsamongphenologicalstudies.The schemehas
levelis thecentralone,corresponding
functional
and geneticalentitiesin a population.At wide applicationnot only for othercharactersof
but
the individuallevel,long timeseriesfromtagged plant phenology,such as leafingand fruiting,
forstudyingphysiological also foranimal phenologyas well. It should now
information
treesfurnish
cues be possibleto addresstemporalquestionsaboutthe
suchas responseto environmental
mechanisms
in thecontextofdifferencesecologyand evolutionof tropicalplant-animalinor endogenousrhythms
withmoreprecision.
in age, size, geneticalcomposition,
gender,or mi- teractions
crohabitat.The subindividuallevels,flower,inflorescences,and branchallow the behaviorof individuals to be analyzed more closely. At the ACKNOWLEDGMENTS
can be made for
populationlevel, interpretations
We thankD. G. Lloydand L. McDade forreviewing
as well as aspects this
pollinationand dispersalsystems,
Forhelpful
criticism
ofearlier
manuscript.
versions
biologysuch as of thisclassification
of demographyand reproductive
we aregrateful
to K. S. Bawa,R.
plant matingsystemsand gene flow.At the guild Borchert,
R. Colwell,
E. 0. Guerrant,
P. Hall,S. Koptur,
andF. G. Stiles.We
J.Rosenthal,
level,thegroupofplantspeciessharedbyonegroup S. Naeem,G. Orians,
R. Echeveria,
C. Esquivel,G. Hartshows thankJ. Frankie,
of animalssuch as pollinatorsor frugivores
in recording
and F. G. Stilesforassistance
shorn,
obserfactors
have vations,
howbroaderecologicaland evolutionary
collection
ofdata,andverifying
monitoring
speofplant-animalinteractions. ciesnames.OTS and NSF fundeddata collection.Funding
led to theorganization
andanalyses
wasprovided
byOTS, NSF,
At the communitylevel,questionsof community fordataentry
at theUniversity
ofEntomology
of
can be ad- andtheDepartment
ecology,biogeography,and floristics
California,
assisted
withdataentry
Berkeley.
J. Barthell
dressed.
andverification.
G. Casterline,
S. Jacobson,
T. Porco,and
In summary,we propose a new classificationP. Spector
consultation
forstatistical
and
kindly
provided
to resolveseveralproblems graphical
forphenological
methods.
patterns

LITERATURE CITED
E., AND P. A. HUXLEY. 1990. The applicationof phenologyto agro-forestry
research.ICRAF Working
Paper No. 63: 1-50.
APPANAH, S. 1982. Pollinationof androdioeciousXerosperrnum
intermedium
Radlk. (Sapindaceae) in a rainforest.
Biol. J. Linn. Soc. 18: 11-34.
1985. Generalflowering
in the climaxrain forestsof South-eastAsia. J. Trop. Ecol. 1: 225-240.
1990. Plant-pollinator
in a Malaysianrain forest.In K. S. Bawa and M. Hadley (Eds.).
interactions
Reproductivebiologyof tropicalforestplants,pp. 85-101. UNESCO and Parthenon,Paris, Franceand
Carnforth,
England.
Malays. For. 44: 234-252.
, AND H. T. CHAN. 1981. Thrips:the pollinatorsof some dipterocarps.
ASHTON, P. S. 1988. Dipterocarpbiologyas a window to the understanding
of tropicalforeststructure.
Annu.
Rev. Ecol. Syst. 19: 347-370.
, T. GIVNISH, AND S. APPANAH. 1988. Staggeredflowering
in the Dipterocarpaceae:
new insightsintofloral
inductionand the evolutionof mast fruiting
in the aseasonaltropics.Am. Nat. 132: 42-66.
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APPENDIX:

TERMINOLOGY

patterns.
Quantitativedescriptions
definedand consistently
used termsfordescribing
Tropicalphenologylacksprecisely
willbe published
duration,amplitude,date,and synchrony
regularity,
of thepatternsusingthevariablesoffrequency,
independent,we are conductinga studyof theirinter-relationship.
elsewhere.As thesevariablesare not necessarily
and fruiting)
To avoid proliferation
of newtermswe use thesame termsforanyphenologicalevent(leafing,flowering,
in thefollowing
can be substitutedforflowering
leafingand fruiting
and forpatternsat all levelsof analysis;therefore,
definitions.We have avoided using termsthat introduceconfusionwith literaturefromotherfieldssuch as tree
of oscillationsin physics.For thisreason,the termsperiod,periodic
and the description
development,chronobiology,
as used in timeseriesanalysis.The
and phase are not used here.We preferto retaintheirmathematicaldefinitions
of flowering
and nonflowering
intervalreplacethedefinitions
phase
definitions
of flowering
episodeand nonflowering
given in Newstromet al. (1993).
on a tree,or flowering
or intensity
of response,such as numberof flowers
Amplitude is the quantityof activity,
amplitude
episodemayhave multipleflowering
A flowering
treesin a population,or speciesin a guild or community.
(e.g., Frankieet al. 1974, Opler et al.
peaks which can be measuredor estimatedqualitativelyor quantitatively
plants
however,may be practicalonlyin understory
1980, Augspurger1983). Countingnumberof inflorescences,
obscuremoresubtlefluctuations.
ariseshereas broadercategories
(e.g.,Bullocketal. 1983). The problemofresolution
episode
Cycle refersto the repeatingsequence of an eventthat is "on" and then "off' such as a flowering
followedby a nonflowering
interval.Each repetition
of thecyclemaybe variablein length(as in subannualflowering)
patterns,a largercycle
or nearlyequivalent(as in annualflowering).
For some of the morecomplexannualflowering
intervalswithinit, whichwe refer
of one majorflowering
episode per yearcontainsbrief"pauses" of nonflowering
to as the pulsed annualpatternafterOliveira et al. (1991). Monocarpicplantsdo not have repeatingcyclesat the
Foster1977; and some
cycleper lifetime(e.g., Tachigalia versicolor,
individuallevelbut ratheronlyone reproductive
bamboo species,Janzen 1976).
categoriesof
Duration is the lengthof timea unitremainsin a givenportionof the cycle.In our classification,
durationforflowering
(> 1 mo and < 5 mo), and extended(> 5 mo). The
episodesare brief(< 1 mo), intermediate
episode or
the durationof flowering
problemof resolutionarisesbecause a long censusintervalwill overestimate
of the numberof cyclesper unit time. Daily observationsare
nonflowering
intervalleadingto an underestimation
usuallyimpractical,however,and a 2 wk or 1 mo censusintervalis commonlyused in phenology.
episode.
Episode is the portionof the cycleduringwhichthe eventis "on" such as flowering
classesbased on an annual
frequency
Frequency is the numberof cyclesper unittime.We definedfourarbitrary
time scale:
continual= alwaysin flowerwith no or fewbriefinterruptions;
subannual= > 1 cycleper year;

Plant Phenology

159

annual = 1 cycleper year;and


supra-annual= multi-year
cycles.
Withinthecontinualclass,a continuous patternmeansthatthereare no interruptions
at all but thisis notcommon
at the individualand populationlevels.Within the supra-annualclass,morefrequentflowering
patternswith 1 to
with 1 to 3 yrofnonflowering
3 yrof flowering
interspersed
belongto thesubclassalternate and infrequent
flowering
patternsbelongto the subclassrare.
Interval is the portionof the cycleduringwhich the eventis "off' such as a nonflowering
interval.At the
populationor guild levelsthisintervalcan also be referred
to as a gap.
Regularity is the variabilityin lengthof cyclesor portionsof the cycles.Regularpatterns,
like annualflowering,
have approximately
equivalentcyclelengthsand the "on" and "off"portionsof the cycletend to be consistentin
durationfromyearto year.Irregularpatterns,like subannualflowering,
have variabledurationsof both the entire
cycleand portionsof the cycle.We are comparingquantitativemethodsfordescribingregularity
(e.g., time series
analysisand othermethodssuch as thosein Colwell 1974, Putz 1979, Raveh & Tapiero 1980, Stearns1981).
Seasonal refersto the temporalassociationof an eventwith a recognizableclimaticseason. While an annual
patternis alwaysseasonalin our data, thetermannualrefers
to frequency
(1 cycle/yr)
notto seasonality.
Forexample,
supra-annualpatternsmay or may not have seasonalassociations.
Date is the calendartime in days, months,or season of the yearwhen the eventoccurs.It is an important
can be measured
reference
point forrelatingplant phenologyto externalabiotic or biotic cycles.Date of flowering
each reflecting
forfirstonset,or maximum,modal, or last flowering;
different
propertiesof the plant'sreproductive
effort
(Primack 1985).
of the same eventin mostor all of the unitsbeing considered(e.g.,
Synchronyis the simultaneousoccurrence
have been used
flowerson a treeor flowering
treesin a population).Different
quantitativemeasuresof synchrony
(Primack 1980, Lack 1982, Augspurger1983, Wright 1991).