Down-Facing Flowers, Hummingbirds and Rain

Author(s): Marcelo A. Aizen

Source: Taxon, Vol. 52, No. 4 (Nov., 2003), pp. 675-680
Published by: International Association for Plant Taxonomy (IAPT)
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2003:675-680
TAXON 52 - November

Aizen * Down-facingflowers,hummingbirds
and rain

and rain
Down-facingflowers,hummingbirds
Marcelo A. Aizen
Laboratorio Ecotono, CentroRegional UniversitarioBariloche, UniversidadNacional del Comahue, Quintral
1250, 8400 San Carlos de Bariloche, Rio Negro,Argentina.marcito@crub.uncoma.edu.ar
Flower orientation,the angle between a flower's main axis and the horizontal,is an importantbut understud-

andrain,and
betweenflowerorientation,
ied flowertrait.I exploretherelationship
hummingbird
pollination,

review evidence forthe adaptive significanceof a down-facingorientationas a mechanismto avoid flower

flooding.A screeningof a tropicaland a temperateflora showed thathummingbirdflowersmore commonly
face down thaninsectflowers.In the temperateforestsof southernSouthAmerica,genera pollinatedby hummingbirdsand genera with down-facingflowers irrespectiveof pollinationmode increase along a strong
E-W precipitationgradientacross theAndes. These patternssuggestthatflowerswitha down-facingorientation are associated with pollinatorsthat,like hummingbirds,remain active duringrain and thatthis type of
flowerorientationmay constitutean adaptationagainst the deleteriouseffectsof nectar dilutionand pollen
rainwash. Still scarce experimentalevidence confirmsthata down-facingmorphologymay preventflower
flooding.However, othermorphologicaltraits,like corolla closure and a narrowtubularshape, could also be

in hindering
effective
nectardilutionandpollenrainwash.

KEYWORDS: adaptation,flowerorientation,hummingbirds,
pollination,rain,South America.

E INTRODUCTION

& al., 1996),hereI

times(Hurlbert
handling
ingflower
thatdown-facing
testpredictions
basedon thepremise
a flower's flowers
and
Flowerorientation-the
exposedto raincan avoidnectardilution
anglebetween
from
anthers
andstigmas.
mainaxisandthehorizontal-is
an important
morpho- pollenrainwash
on flower
Theselective
influence
ofabioticfactors
remains
whoseadaptive
largely
significance
logicaltrait
is an aspectoffloral
thathasbeen
Thistrait
andwithin morphology
variesmarkedly
biology
among
unexplored.
but
biologists,
bymodempollination
neglected
lifespan mostly
planttaxa,andevencanchangeovera flower's
in
(see references
(Huang& al., 2002). Examplesof speciesandgenera notby earlyEuropeannaturalists
C.K. Sprengel
flowersthateitherface Corbet,
century
1990).As earlyas the18th
animal-pollinated
producing
onflower
andfertilization
structure
or"downwards"
canbe foundinpractically inhistreatise
(1793;
"upwards"
indetail
inLloyd& Barrett,
all mainplantfamilies
1996)explained
(i.e.,Asteraceae,
Papilionaceae, translated
havetoavoidnectar
thatflower themanymechanisms
diluflowers
Acanthaceae,
Solanaceae,
etc.).Thissuggests
he wrote
canshift
ofa plant tionbyrain.Regarding
orientation
flowers,
down-facing
easilyalongtheevolution
withparticular
theouterside
inassociation
flowers]
present
polli- (p.14)"They[pendulous
lineage,
specifically
thefalling
theinner
sideis exposed
to
modes(seeBruneau,
nation
raindrops;
1997).Forinstance,
hanging toward
iftheyarebell-shaped
or
flowers
flowers
exhibiting
negative littleor no rain,particularly
(andmoregenerally
is locatorspherical
tothehorizontal)
shape.Thenectar
appeartooccurfre- havea cylindrical
angleswithrespect
where
theraindrops
flowers.
This edabove(atthebaseoftheflowers),
quentlyamonghummingbird-pollinated
ofscent,
Theseflowers
and cannotascendbecauseoftheirweight...
tubular
trait,
shape,absence
plusredcolour,
weather".
of largeamounts
of dilutednectarrichin donotneedtocloseinrainy
production
morethantwocenturies,
weknowlittle
ofhow
definetheso-called"hummingbird-pollinationAfter
sucrose,
a down-facing
is inavoidflower
& al., 1996). efficient
1968;Proctor
morphology
(Grant& Grant,
syndrome"
overallplantfit"down- ingnectar
whichcandecrease
itis unclearwhyandto whatextent
dilution,
However,
discriminative
dilution
shoulddeter
occursmuchmorefrequently
pollinaamonghumming- ness.Nectar
facing"
kindof torsfromvisiting
hencedecreasing
visitation
thanamongflowers
visited
birdflowers
flowers,
byother
andpollen
ontostigmas,
insects.
frequencies,
pollendeposition
particularly
pollinators,
from
boththefemale
ofa
removal
anthers.
As a result,
theadaptive
Inthisassay,I explore
(seed
significance
ofplantfitness
in relationto rain. set)andmale(seedsiring)
flowerorientation
components
down-facing
In addition,
a hanging
flower
petalsin down-facing
efficiency shouldbe affected.
mayalsoincrease
Although
couldactas "umbrellas",
inpollentransfer
pollenfrom
protecting
byincreas- flowers
bypollinators,
particularly
675

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and rain
Aizen * Down-facingflowers,hummingbirds

TAXON 52 November2003: XX-XY

lowerthan
and stigmas(i.e., the theChiloesite(-2800mm)beingsomewhat
fromanthers
beingrainwashed
airhumidity
isveryhighyear-round
dueto
hypothesis";
Tadey& Aizen,2001). atAntillanca,
"pollen-protection
was
to thePacificOcean.Flowerorientation
thefrac- proximity
coulddecrease
anthers
Direct
pollenlossesfrom
to oneof twocategories
available assigned
andtheamount
tionofpollenthatis exported
(either
up-ordownand/or
field
direct
& Smith,
forfertilization
) basedonflower
photographs
2001).Pollen facing
(see alsoBynum
wererepresented
Mostgenera
andgerminabilityobservations.
itsviability
couldalso affect
byjustone
wetting
and in thefewinstances
speciesat a singlelocality,
(Huang& al.,2002).
related
to wheremorethanone speciespergenusoccurred
newevidence
Here,I reviewandprovide
they
orientation.
flood- hadthesametypeofflower
derived
from
thefollowing
Changesinthe
Sprengel's
predictions
withdown-facing
flowers
ofgenera
alongthis
proportion
hypotheses:
ingandthepollen-protection
for
wasassessedusingregression
should
berelative- E-Wgradient
flowers
1.Taxawithdown-facing
analysis
and categorical
data(seeAizen& Ezcurra,
inhigh-precipitation
environments
1998,formethodlymorecommon
thatremain
active ologicaldetails).
withvertebrate
associated
pollinators
an
andI conducted
InMay2002a groupofstudents
rain,suchas hummingbirds.
during
at Los AmigosConservation
thatfacedownshould experiment
a species,flowers
2. Within
Area,Peru,in
5 mmofrainfall
on fresh
cutflowrainthanflowers whichwe simulated
havetheirnectarless dilutedduring
Besleria sprucei
ers of hummingbird-pollinated
thatfaceup.
a largeherbthattypically
anthers (Gesneriaceae),
a species,
direct
3. Within
produces
pollenlossesfrom
flowers
inup-thandown-facing down-facing
andstigmas
shouldbe greater
(Fig.la). We appliedthreetreatnatural
flowers
heldattheir
ments:
flowers.
average
down-facing
while
orientation
(~ -70 relativeto the horizontal)
heldup-facing
(- +70) while
exposedtorain,flowers
notexposedto rain.Rain
exposedto rain,andflowers
AND METHODS
MATERIALS
wassimulated
perforausinga plasticglasswithminute
I conducted
ofthetropical
a screening
(in %
(Amazonian) tions.Nectarvolume(in pl) and concentration
inflowers
weremeasured
Conservation
flora
ofLosAmigos
rainforest
Area,Madre sucroseequivalents)
sampled
de Dios, PerN(1234' S, 70006'W) (R. Foster,H. Betz, after15, 60, 120, 360 minusingcalibrated
capillary
rain- tubesanda handrefractometer,
andthetemperate
R.Burnham,
(-10 flowrespectively
(Valdivian)
unpubl.)
x timecombination).
Nectarvariables
erspertreatment
floraofPuertoBlest,Rio Negro,Argentina
forest
(4108'
ANOVAwithtreatment
usinga two-way
S, 7148'W; Brion& al., 1988).Basedonphotographswereanalyzed
Volumewas transformed
as
flower
orinflorescence
images(92 and andtimeas fixedfactors.
close-up
showing
andhomoscedasofnormality
42 speciesforLosAmigosandPuerto
Blest,respective- log(x+1)tomeetcriteria
theproportion
ofspecieswithdown-fac- ticity
(Sokal& Rohlf,1981).
ly),I estimated
onavershowing,
(i.e.,specieswithflowers
ingflowers
to thehorizontal)
amonghumage,angles<0 relative
andinsect-pollinated
woodyplants(see also
mingbird* DOWN-FACING FLOWERS, HUMpolliTadey& Aizen,2002).InthecaseofLosAmigos,
MINGBIRDSAND RAIN
natortypewas assumedbased on flowershapeand
are themostimportant
vertebrate
inthefloraof
& al., 1996)whereas
colour(e.g.,Proctor
Hummingbirds
intheNewWorld.
was based on published pollinators
PuertoBlest,classification
bythese
Speciespollinated
a sizablepercent
ofmanytropical
of flowervisitors(Smith- vertebrates
accountson the identity
represent
florasin theAmericas(Grant&
& Armesto,1994; and eventemperate
Ramirez,1993; Smith-Ramirez
cat- Grant,1968; Gentry,1982; Aizen & al., 2002).
between
2002).Differences
Vazquez& Simberloff,
underheavyrain,and
areabletoforage
ExactTest.
wereassessedbyFisher's
Hummingbirds
egories
andhum- even duringsnowfalls(Burton,2001). Furthermore,
theproportion
ofinsectI also estimated
anddonot
flowers
aregenerally
exhibit- hummingbird
withflowers
long-lived
woodygenera
mingbird-pollinated
a down-facrain(pers.observ.).
Llao- closeduring
Therefore,
(Bariloche,
anglesat fivelocalities
ingnegative
becommon
should
andChiloe)distributedingmorphology
among
hummingbird
Llao, PuertoBlest,Antillanca,
acrosstheAndes flowers.
E-W rainfall
gradient
alonga strong
thetropical
ofLosAmigos
Inbothrainforest
40 and42S,basedonthelistofplantgenera
between
floras,
ofPuertoBlest,> 85% ofthehumbetween andthetemperate
(1998).Distance
byAizen& Ezcurra
compiled
flowtheeasternmost
site(Bariloche)to thePacificOcean mingbird-pollinated
down-facing
speciesproduce
meanangles< 0 withrespect
tothe
800mm ers(i.e.,exhibiting
from
ranges
(Chiloe)is about230km.Rainfall
< 35%oftheinsect-pollinated
at horizontal).
As a contrast,
atBariloche
to4000mmatAntillanca.
Despiterainfall

676

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TAXON 52 November2003: 675-680

Aizen * Down-facing flowers, hummingbirds and rain

foreffectsof rainon nectarand pollen.A, a flowerof Besleria sprucei (over deveFig. 1. Species tested experimentally
lopment, flowers bend from a slightly down-facing position, as shown, to an - -70; B, a pendant inflorescence of
Tristerixcorymbosus showing their down-facing flowers.

LOS AMIGOS
100
(I)
0
0

P < 0.001

80
60
40

C
0
'ID

n=60

20
0

Insects

Hummingbirds

Pollinator
type
PUERTO BLEST
Cn
(D
B

100

m
.5

60

40

20

P < 0.01

80

n =-A

00

Insects

Hummingbirds

Pollinatortype
Fig. 2. Proportion of species with flowers exhibiting
negative angles (< 0) among hummingbird- and insectpollinated woody plants in the Amazonian flora of Los
Amigos Conservation Area, Madre de Dios, Peru and the
temperate flora of Puerto Blest, Rio Negro, Argentina.
Differences between categories were assessed
by
Fisher's Exact Test.

speciesin thosetwolocalitiesproduceflowersshowing
a down-facing
orientation
(Fig. 2). Theseresultsdemonstratea strongassociationbetweenhummingbird
pollinationanda down-facing
flowermorphology,
independentof phylogeny
as littletaxonomicrelationship
exists
betweenmostoftheomithophilous
speciesofthesetwo
floras(pers. observ.).However,these resultscannot
demonstrate
thatrainis theultimate
selectivefactorlinkflowersandhummingbirds.
ingdown-facing
ifbothhummingbird
Thislinkcouldbe strengthened
flowersand a down-facing
floralmorphology,
irrespective of animalpollinationmode,were associatedwith
habitats.Hummingbird
flowers(and
high-precipitation
are indeedcommonin many
themselves)
hummingbirds
cloudandrainforest
andother
communities,
Neotropical
wet habitats(Stiles, 1981; Gentry,1982; Aizen & al.,
2002). However, quantitativecomparisonsare still
scarce. Examinationof changesin pollinationmodes
amongwoody generaalong the precipitation
gradient
describedabove showsa strongincreasein theproportion of woody generawithhummingbird-type
flowers
(from-5% to> 20%) fromtheeasternmost
(xeric)to the
westernmost
forest
(mesic)boundariesof thetemperate
of southernSouthAmerica(Aizen & Ezcurra,1998).
on flowerorientation
to thisdataset
Addinginformation
shows thatthe proportion
of hummingbird-pollinated
flowerswas highanddid
generaproducing
down-facing
not changesignificantly
the entiregradient
throughout
(Fig. 3). This mightbe expectedas thefewhummingtaxa presentin theforesteast of theAndes
bird-flower
werealso presentin themorerichhummingbird
forest
florawestoftheAndes(Aizen& al., 2002). Moreinterof generawitha down-facestingis thattheproportion
taxa increases
ing morphology
amonginsect-pollinated
two-fold(fromabout20 to 40%) fromE to W (Fig. 3).
677

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TAXON 52 - November2003: 675-680

Aizen * Down-facingflowers,hummingbirds
and rain

aftertreatment
showedthatthisstrong
nectardilution
effect
foratleast6 h (Fig.4). Indeed,
lastedunchanged
o 80
- Humming- inthisprotandrous
life
speciesrainfalling
earlyinflower
bird
C)
couldaffect
nectar
fortheentire
flower
quality
lifespan
60
c
thesedatasuggest
thata down-facing
(-2 d). Therefore,
in preventing
is effective
flower
morphology
flooding.
whattheconsequences
areofnectar
dilution
However,
a0
on
behaviour
in this
and
hummingbird
pollination
20
o
unknown.
speciesremain
offlower
infloresManipulation
anglesin pendant
cencesofthehummingbird-pollinated
mistletoe
Tristerix
W-Egradient
corymbosus
(Loranthaceae)
(Fig.lb) exposedtonatural
teththatflowers
(Tadey& Aizen,2001)showed
Fig. 3. Proportionof insect-and hummingbird-pollinated rainfall
ered to face up did not have theirnectardiluted.
woody genera withflowersexhibitingnegativeangles at
fivesites located along a strong E-W rainfallgradientin
Avoidance
ofwater
entrance
intothecorollamight
relate
the northernportionof the temperateforestsof southern to thenarrow
tubularshapeof theflowers
also
(see
South America(40-420S). Distance betweenthe easternRain
the
affected
number
of
Corbet,
1990).
strongly
most,driestsite (Bariloche) to the PacificOcean is about
in thestyles.However,
up-facing
230 km. The proportionof genera withdown-facingflo- pollentubescounted
Q) 100

Insect

.,_

fromeast to west (regressiwers increased significantly

on analysis for categorical data, x2 = 5.84, P = 0.0156)
among insect-pollinatedplanttaxa, whereas the longitudinal trend for hummingbird-pollinated
genera was not
significant(X2= 0.02, P = 0.89).

2.0
+
-I

a
that(1) rainmayconstitute
Theseassociations
suggest
an ecological
directselectiveagent(or alternatively
flowermorphology,
and (2)
sieve)fora down-facing
whicharepredominately
characflowers,
hummingbird
terizedby this trait,thrivein wet environments.
thefirst
basedonpreliminary
evidence,
preTherefore,
aboveis clearly
diction
stated
supported.

=3

0
._1

1.5

I-..

,+-- I.-

1.0

0.5
0.0

II

15

60

120

360

Time (min)
-- Down-facing
Up-facing

-4*A

E MANIPULATIVEEXPERIMENTS

Control

30
25

....,,
0
Scarceevidenceexistson how flowerorientation
20
andpollinaaffects
nectar
visitation,
dilution,
pollinator
0- 15
a down-facing
corollamaypretioneventsorwhether
10
Thislackofresearch
ventpollenfrom
beingrainwashed.
0
5
is a trait
that
becauseflower
orientation
is quitestriking
o
z.z----_.
_..-0
T
rI-insomeflowers
of
canbe easilymanipulated,
although
15
60
120
360
generasuchas Fuchsia(pers.observ.)or Pulsatilla
oftheflower
cannot
bepre(Huang& al.,2002)bending
Time (min)
vented.
ofnectar
toartificial Fig. 4. Mean (+ 1 SE) nectarvolume(shown as log [ x + 1])
after
right
exposition
Sampling
rainonflowers
ofBesleriasprucei
heldatnatural
angles and concentration(in % sucrose equivalents) of Besleria
in flowersexposed to artificialrainwhile held eitherup- or
(-70)didnotshowanyevidenceofnectardilution
down-faced.Control flowerswere not
to rain.
notexposed
torain(meanvolume Flowers were sampled at either15, 60,exposed
toflowers
comparison
120, or 360 min
c

+ 1SE = 4.2 + 2.32 vs. 3.4 1.63 gl, andmeanconcen-

aftersimulatedrain.Treatmenthad significanteffectson
both nectarvolume and concentration(F2,110= 46.84, P <
while 0.0001 and F2,83=152.07, P < 0.0001, respectively),wheOn theother,
flowers
heldup-faced
equivalent).
of time (F3,110= 0.29, P = 0.83 and F3,83=
rainbecameflooded
(91.2 43.74 reas effects
exposedto artificial
P = 0.68) and treatmentx time interaction(F6,110=
0.50,
volumeandconcentration,0.89, P = 0.50 and
gl and0.6 0.31%fornectar
F6,83= 0.63, P = 0.71) were not signifiatdifferent
times cant.
Besleriaflowers
respectively).
sampled

trationi 1SE = 19.4 1.10 vs. 18.8 2.78 % sucrose

678

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TAXON 52 November2003: 675-680

flowersdidnotshowevidenceofdifferential
pollenlossto
es fromanthers
andstigmasdueto rainin comparison
flowers.Finally,
or manipulated
naturally
down-facing
had any
neitherexposureto rainnorflowerorientation
to expectations,
resultsof
effecton seed set. Contrary
this experimental
studyshow thatin this mistletoea
for
is inconsequential
flowerorientation
down-facing
avoidingthe deleteriouseffectof rain on pollination.
damOtherstudiesshowthatraincan cause irreversible
age to anthersand to pollenin some species(see referthis
ences in Corbet,1990),butit is unknownwhether
effect
can be ameliorated
by flowersfacingdown.
flowerclosurecan represent
Temperature-induced
anotherversionof the corolla's umbrellaeffect.For
instance,flowersof Gentianaalgida close theircorolla
as a responseto a temperature
dropthataccompanies
commonin the alpine habitatof the
thunderstorms,
of corollaclosuredurprevention
species.Experimental
ingrainnotonlyincreasedpollenrainwashfromanthers
but also decreasedseed set,probablyassociatedwith
pollendislodgingfromthestigmaandpollendamageby
rain(Bynum& Smith,2001).

CONCLUDING

REMARKS

the still scarce experimental

eviTaken together,
can
dencereviewedheresuggeststhatflowerorientation
inavoidingflowerfloodingandnectardilube important
traitcan be particularly
tion.This morphological
adapcorollathroats
tiveinflowerswithwideormedium-sized
likethoseofBesleria.Othermorphological
traitssuchas
presenceof hairsinsidecorollas,or a narrowtubular
alternative
mechanismsto avoid
shape may constitute
nectardilutionby rain(Corbet,1990; Bertin& Sholes,
1993; Tadey& Aizen,2001). Evidencethata down-facis criticalforavoidingdirectpollenlossingmorphology
es fromanthers
and stigmasis stillequivocal.At leastin
flowerswithextrudedsexualpartsas thoseof Tristerix,
umbrellas.
corollasdo notactas effective
I foundevidencethata down-facing
morphology
was strongly
associatedwithhummingbirds,
i.e.,pollinatorsthatforageactivelyduringrain.It is also likelythat
directagentsof selection
hummingbirds
mayconstitute
flowermorphology
to theextentthat
fora down-facing
and
enhancespollen transfer
this type of orientation
&
deterspollination
byotherbioticagents(e.g.,Hurlbert
flowers
al., 1996). However,thefactthatdown-facing
ofaniseemtobe commoninrainyhabitats,
independent
mal pollinationmode,makesit likelythatrainfallcan
their
becomea strongselectiveagentforplantsorienting
flowersfacingdown.In thiscase, therelationbetween
and flowerswithnegativeanglescould
hummingbirds
of strongdirectassociationsof
theby-product
represent

Aizen * Down-facingflowers,hummingbirds
and rain

bothhummingbirds
and plantsproducingdown-facing
flowerswithrainyhabitats.

ACKNOWLEDGEMENTS

I thankMarisol Amaya, Dawn Frame, and Gerhard

fortheirkindinvitation
in thesympoto participate
Gottsberger
sium"La interacci6n
enrelaci6n
a la morfologia
floplanta-animal
ral"heldduring
theVIII CongresoLatinoamericano
de Botanica,
Cartagenade Indias,Colombia.My thanksalso to Robinson
JoseFlores,Clementina
Botero,
Gonzalez,AnitaHorta,andDiana
Ramos, studentsof the course Ecologia de Ecosistemas
Amaz6nicos
in thedesignand
(OTS 2002-13),whocollaborated
oftheBesleriaexperiment,
andto CeciliaEzcurra,
development
Cecilia Smith-Ramirez
and two anonymous
reviewers
fortheir
critical
ofthemanuscript
andusefulsuggestions.
reading

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