Leaf Ultraviolet Optical Properties Along a Latitudinal Gradient in the Arctic-Alpine Life Zone

Author(s): Ronald Robberecht, Martyn M. Caldwell and W. D. Billings

Source: Ecology, Vol. 61, No. 3 (Jun., 1980), pp. 612-619
Published by: Ecological Society of America
Stable URL: http://www.jstor.org/stable/1937427
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Ecology, 61(3), 1980, pp. 612-619
? 1980 by the Ecological Society of America

LEAF ULTRAVIOLET OPTICAL PROPERTIES ALONG A

LATITUDINAL GRADIENT IN THE
ARCTIC-ALPINE LIFE ZONE'

RONALD ROBBERECHT AND MARTYN M. CALDWELL

Departmentof Range Science and the Ecology Center,
Utah State University,Logan, Utah 84322 USA

AND

W. D. BILLINGS
Departmentof Botany, Duke University,
Durham, North Carolina 27706 USA

Abstract. Leaf epidermaltransmittanceof terrestrialsolar ultraviolet-Bradiation(295-320 nm)

was examined along a latitudinalgradientof solar UV-B radiation. In high UV-B radiationzones,
e.g., equatorial and tropicalregions,mean epidermaltransmittance forthe species examined was less
than 2%. At higherlatitudes,mean epidermaltransmittanceexceeded 5%. Althoughthis latitudinal
solar UV-B gradientrepresentsmorethana seven-folddifferencein daily integratedUV-B irradiance,
the calculated mean effectiveUV-B irradianceat the mesophyllof low-latitudespecies is not sub-
stantiallydifferent fromthat of species at higherlatitudes. Species in high UV-B radiationenviron-
mentsappear to attenuatethisradiationmoreeffectively thanthose in lower irradianceenvironments.
In mostcases, absorptionof UV-B in theepidermisis the majorparametereffecting low transmittance.
Reflectancefromglabrous leaves is generallyless than 10%. In some species, pubescent or glaucous
leaf surfacescan reflectmore than 40% of the UV-B radiationincidenton a horizontalleaf, although
such surface characteristicsdo not necessarily indicate high UV-B reflectance.Under controlled
conditions,epidermaltransmittancein Pisum sativum L. decreased in response to UV-B irradiation.
The modificationof epidermaltransmittance,resultingin lower UV-B irradianceat the mesophyll,
may representa mechanism of plant acclimation to UV-B radiation. Such acclimation may have
occurred in several wildland species of temperate-latitudeoriginthat have invaded highUV-B irra-
diance equatorial and tropicalregions.
Key words: absorptance; arctic-alpineenvironments;epidermal transmittance;leaf epidermis;
leaf optical properties:reflectance;ultravioletradiation.

INTRODUCTION ingto its effectivenessforDNA damage (Setlow 1974),

maximum effectiveUV-B irradiance between these
Solar ultravioletradiation,UV, can be a significant
environmentalstressfactorforthe growthand devel- zones differedby more than an order of magnitude
opmentof sensitiveplants (Caldwell 1971,Bogenried- and total daily effectiveradiation differedby more
er and Klein 1977, Sisson and Caldwell 1977). Al- than seven-fold,withthe highestvalues in hightrop-
thoughthe energyreceived in the UV-B portionof the ical mountains.This differenceconsiderablyexceeds
terrestrialsolar spectrum(295-320 nm) is less than any increase in UV-B irradianceat temperatelatitudes
0.5% of the total shortwave flux incident on the predictedto resultfromman-causeddisturbanceofthe
Earth's surface,radiationat these wavelengthsis ca- stratosphericozone layer, the primaryabsorber of
pable of inducingdisruptivephotochemicalreactions shortwaveUV radiation(Hudson 1977). In contrast,
in plants. Changes in the molecular structureof nu- the total daily solar shortwaveradiationfluxfordays
of maximumsolar irradiationwas found to be about
cleic acids and proteinsin the leaf (Murphy 1975), as
well as injuryto the photosynthetic the same throughoutthis gradient.Given the magni-
apparatusand leaf
tissues, may occur in sensitiveplantsupon absorptiontude of the latitudinalUV-B radiationgradientand the
of UV-B radiation(Sisson and Caldwell 1976, Brandle actinic nature of radiation in this waveband, an ex-
et al. 1977). amination of plant species from a similar life zone
A previous paper demonstrateda pronounced lati- along this gradientcould provide insighton mecha-
tudinalgradientof UV-B radiationin the arctic-alpinenisms of plant adaptationto UV-B radiation.
life zone fromthe equatorial mountainsto 'thearctic Attenuationof UV-B radiation by the cuticle and
tundra(Caldwell et al. 1980). When weightedaccord- epidermismay be a mechanismfor reducingthe UV-
B fluxincidentat the mesophylllayer. The potential
1 Manuscriptreceived22 June1979;accepted2 October of the epidermallayerto alterthe qualityand quantity
1979;finalversionreceived29 October1979. of incidentUV radiationled to the selection of epi-

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June 1980 LEAF UV OPTICAL PROPERTIES 613

dermal transmittanceas a parameter to measure in mesophyllmaterial,as determinedby microscopicin-

species occurringalong this latitudinalgradient.More spection, was used. The tissue was placed in contact
effectiveattenuation,i.e., reduced epidermal UV-B with moistened filterpaper and immediatelyposi-
transmittance,may be concomitantwiththe trendof tioned over the entranceport of an integrating sphere
increasing UV-B radiation from arctic to equatorial forthe measurementof UV transmittance.
latitudes.If such a trendin epidermalattenuationex- A small integratingsphere, coated with "Halon"
ists, the solar UV-B flux at the mesophyll layer of (Diano Corporation), a nearly perfect reflectorand
species in high irradiance environmentswould not diffuserof UV radiation (Venable and Kostkowski
necessarilybe greaterthan for species in low UV-ir- 1975), was used to measure both the obliquely scat-
radiance habitats. tered and direct beam radiationtransmittedthrough
Vegetation of the arctic-alpine life zone of the the sample. The integratingsphere was coupled to a
NorthernHemispherewas selected for studybecause Gamma CorporationgratingmonochromatorGC-700-
thiszone spans the entirelatitudinalgradient,fromthe 31 and photometerGC-2900. Measurementsof trans-
polar regions to upper elevations of temperateand mittanceand reflectancewere made, relativeto a Hal-
equatorial mountainranges (see Caldwell et al. 1980). on standard,at 5 and 10 nm intervalsover the 290 to
Along this latitudinalarctic-alpinegradient,thereare 400 nm waveband. Reflectancewas measured on the
strongsimilaritiesin certainecosystemicfactorssuch upper surfaceof intactleaf disks. Except for a modi-
as low air temperaturesduringthe growingseason, ficationto allow the measurementof reflectance,the
and similarplant growthforms(Billings and Mooney integratingsphere/spectroradiometer system used in
1968, Billings 1974, Billings 1979). Several major arc-
the presentstudyis identicalto thatdescribedby Rob-
tic-alpine sites in Alaska, Utah, Hawaii, and in the berechtand Caldwell (1978). Absorptance was calcu-
Andes of Venezuela and Peru were selected forstudy. lated by subtraction.
In additionto indigenousAndean alpine species, sev- The efficacyof UV-B radiationin biological systems
eral temperate-latitude wildland and agricultural can be described in a meaningfulmannerthroughthe
species were included in this survey. use of action spectra. A generalized action spectrum
for whole plants (Caldwell 1971) and a DNA action
METHODS
spectrum (Setlow 1974) were used as two sets of
Epidermal and leaf UV optical propertymeasure- weightingfunctions(Caldwell et al. 1980) for more
ments of species, mainlyof alpine and arctic tundra biologically relevant measures of epidermal UV-B
lifezones, were made at the five major research sites transmittance.Effectiveirradiance at the mesophyll
noted in Table 1. This plant surveywas composed of (effectivemW/M2), 'mes' was calculated from:
the more abundant species in the plant communityat f320
each research site along the latitudinal gradient. EffectiveTies = T IA- Ex dA
Species endemic to the sites as well as those with 290

broad geographicaldistribution,representingvarious where T. is mean epidermalUV-B transmittance,IA

lifeformsand epidermalcharacteristics,were includ- is the spectral irradiance, and Ex is the biological
ed. Althoughnot the primarycriterionforinclusionin weightingfunctionat wavelengthX. The generalized
the survey,species in which the epidermiswas more plant-and DNA-action spectraare normalizedto unity
readilyremovedwere sampled at a greaterfrequency. at 280 nm and 265 nm, respectively.
All species were collected from exposed habitats. Althoughthe emphasis of this studywas directedto
With the exception of the temperate-latitude species a survey of plants in their natural environment,the
(Logan, Utah), the plantswere examinedin the spring potential phenotypic plasticity of epidermal UV-B
and early summerof 1977. The Logan group was ex- transmittancewas examined in Pisum sativum 'Al-
aminedin Juneand July,1976,as partofanotherstudy derman.' This cultivar, of temperate-latitudeorigin,
(see Robberechtand Caldwell 1978). These latterdata is cultivatedextensivelyin the high mountainvalleys
were adapted for comparison with the plants of the of Peru (Ferry-MorseSeed Company, personal com-
present study and represent the temperate-latitude munication).Seeds ofthiscultivarwere acquired from
measurementsof epidermalUV transmittance. the Ferry-MorseSeed Company, which provides the
Leaf epidermaltransmittanceand reflectancewere Peruvian seed stock. Under greenhouse conditions,
measured on fresh,turgidleaves shortlyafterthe col- where solar UV-B is absent, one group of plants was
lection of whole plants fromthe field. In most cases, exposed to UV-B irradiationemittedfromfilteredUV
five samples per species were measured. Epidermal fluorescentbulbs as described in Sisson and Caldwell
tissue was isolated primarilyby peeling offthe upper (1975). These bulbs do not perfectlysimulatesunlight,
epidermisfromthe leaf. When this was not possible, but do provide some approximationof the spectral
the upper epidermiswas isolated by gentlyscraping distributionof UV-B radiationfromsunlight.The ef-
offthe undersideof the leaf. No chemical agents were fectiveUV-B irradiancelevel was about 2100 effective
used to isolate the epidermis. Only epidermal tissue J-m-2 d-1, when weighted with a generalized plant
at least 3 mmin diameterand freeof perforationsand action spectrum(Caldwell 1971). A controlgroup re-

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614 RONALD ROBBERECHT ET AL. Ecology, Vol. 61, No. 3

TABLE 1. Mean epidermalUV-B transmittanceand the calculated daily effectiveirradiance(J/m2)at the mesophyllof plant
species along a latitudinalgradient.The standard errorof the mean (SE) is given at 305 nm. Planted exotic species or
adventive weeds are indicatedby an asterisk.

Daily fluxat
Mean mesophyll
epidermal (effectiveJ/m2)
UV-B
trans- SE at Biolog-
mittance 305 nm ically DNA
Species (%) (%) effective effective
Equatorial latitudes:
(Peru, 3000-4400 m elevation Platitude10?S)
*Eucalyptus camaldulensis Dehn. 0.1 0.02 2.8 0.2
*Eucalyptusglobulus Labill. 0.1 0.03 2.8 0.2
Wernerianubigena H.B.K. 0.5 0.16 14.0 0.9
Echeveria sp. 0.6 0.35 16.9 1.0
Poa fibriferaPilger 1.0 0.28 28.1 1.8
Salix humboldtianaWilld. 1.1 0.23 30.9 1.9
Oenothera multicaulusR. et Pav. 1.4 0.26 39.3 2.4
*Pisum sativum L. 2.1 0.23 59.0 3.7
Festuca dolichophyllaPresl. 3.0 0.50 84.3 5.2
Perezia multiflora(H.&B.) Less. 3.2 0.59 89.9 5.6
*Medicago hispida Gaertn. 4.7 0.55 132.1 8.2
Taraxacum Sect. Mexicana, A. J. Richard 5.0 0.26 140.5 8.8
*Viciafaba L. 5.8 0.63 163.0 10.2
(Venezuela, 3000-4400 m elevation -latitude10?N)
Espeletia humbertiiCuatr. 0.02 0.01 0.6 0.04
Espeletia schultziiWedd. 0.1 0.00 2.8 0.2
*Eucalyptus tereticornisSm. 0.1 0.07 2.8 0.2
*Oenothera cuprea Schl. 0.7 0.19 19.7 1.2
Senecio greenmanianusHier. 0.9 0.11 25.3 1.6
Echeveria venezuelense Rose 1.0 0.79 28.1 1.8
OritrophiumlimnophilumCuatr. 1.8 0.21 50.6 3.2
Senecio formosus H.B.K. 2.7 0.74 75.9 4.7
Lupinus meridanusMoritz 4.3 0.37 120.8 7.5
Cerastiumracemosum Bartl. 4.3 0.97 120.8 7.5
Senecio funckiiSch. Bip. 5.2 1.71 146.1 9.1
Tropical latitudes:
(Haleakala, Island of Maui, Hawaii, 2500-3000 m
elevation =latitude 20?N)
Sophora chrysophyllaSeem. 0.1 0.03 2.6 0.1
Argyroxiphium sandwicense DC. 0.1 0.03 2.6 0.1
VacciniumreticulatumSm. 0.2 0.06 5.2 0.3
GeraniumtridensHbd. 0.3 0.05 7.8 0.4
*Eucalyptusglobulus Labill. 0.3 0.35 7.8 0.4
Dubautia menziesii (Gray) Keck 0.5 0.05 13.0 0.7
*Rumex acetosella L. 2.5 0.06 64.9 3.6
*Oenothera stricta Ledeb. 4.1 0.62 106.5 5.9
Arcticlatitudes:
(Barrow and Atkasook, Alaska, 2 m elevation
Platitude71?N)
Epilobium latifoliumL. 0.4 0.18 2.3 0.1
Saxifraga hieracifoliaWalst. & Kit. 0.6 0.13 3.4 0.1
EriophorumangustifoliumHonck. subsp. subarcticum
(Vassiljev) Hult. 1.1 0.48 6.2 0.3
Lagotis glauca Gaertn. subsp. minor(Willd.) Hult. 1.3 0.26 7.4 0.3
Oxyriadigyna (L.) Hill 3.2 0.91 18.2 0.8
Petasites frigidus(L.) Franch. 3.8 0.58 21.6 0.9
Parrya nudicaulis (L.) Regel subsp. septentrionalisHult. 4.2 1.20 23.9 1.1
Rumex graminifoliusLamb. 5.4 0.50 30.7 1.3
Ranunculus nivalis L. 6.8 0.89 38.6 1.6
Arctagrostislatifolia(R.Br.) Griseb. var. latifolia 7.0 1.04 39.8 1.7
Ranunculus pygmaeus Wahlenb. subsp. pygmaeus 24.4 2.17 138.6 5.9

ceived no UV-B radiation.Due to overcast skies, pho-
tosyntheticallyactive radiation (400-700 nm) in the
greenhouse was less than 20%oof that normallyinci-
dent duringthe cultivationin Peru.
RESULTS
Mean epidermalUV-B (290-315 nm) transmittance
and the calculated daily UV-B flux incident on the
mesophylllayer are listed in Table 1. The standard

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June 1980 LEAF UV OPTICAL PROPERTIES 615

1E200 ANDES U INCIDENTFLUX

WOO
<= r FLUX
| * AT MESOPHYLL
z

100
w

P-

0
w
20.

Li

PERU VENEZUEAVEEGHAWI UTAALSK

z
4
I--.

320 400 320 400 320 400 320 400 320 400
WAVELENGTH (nm)

FIG. 1. Daily DNA-effectiveUV-B irradiance(J m-2 d-1) at the seasonal maximumfor each location, and the mean
effectiveUV-B flux at the mesophylllayer (mnes)for each species group along a latitudinalgradient(Top). Althoughthe
incidenteffectiveUV-B radiationfluxis considerablyhighernear the Equator comparedto theArctic,a low Imesis maintained.
Epidermalspectra at each location reveal a greaterdegree of variabilityin the magnitudeof transmittance
at higherlatitudes
(Bottom). Note the characteristicspectraldistributionof each species.

errorof the mean is given at 305 nm, a wavelength
that is representativeof the magnitudeof epidermal
transmittanceand the degree of errorassociated with
measurementsin the UV-B waveband. A similarlist
of species occurringin the vicinityof Logan, Utah, is
given in Robberecht and Caldwell (1978). Mean epi-
dermal UV-B transmittanceof equatorial- and tropi-
cal-latitudespecies was less than2%, representingap-
proximatelya 98% attenuationof the UV-B radiation
incidenton a horizontalleaf. At higherlatitudes,mean
epidermal transmittanceincreased, as indicated by
temperate-region and arctic species groups.
Epidermalattenuationsubstantiallyreduces the cal-
culated effectiveUV-B radiation flux reaching the
mesophyllcell layer (Fig. 1). On eithera biologically-
or DNA-effectivebasis Imesis always less than 10%
of the incidentfluxon the leaf. Althoughthe incident
effectivesolar UV-B radiation flux is considerably
greaterat equatorial and tropical latitudescompared
to higherlatitudes, the flux at the mesophylltissue
remainsrelativelylow.
Differences among species in epidermal UV-B
transmittance along the latitudinalgradientcan be dis-
cerned more clearly from epidermal transmittance
spectra (Fig. 1). The spectra are presentedin such a
manneras to convey simultaneouslythe variationin
magnitudeamong species and characteristictransmit-
tance spectra of differentspecies. Epidermal trans-
mittancespectraindicate a greaterdegree of variation
in the magnitudeof UV-B transmittanceof temperate
comparedwithtropicaland equatorial species. A com-
parison of the variance in epidermalUV-B transmit-
tance of the species along the gradientindicate that
the pooled variance of temperateand arctic species is
significantlygreater(forF distribution,P < .05) than
the pooled variance of the equatorial and tropical
species. The F-ratio indicatesthatthe variances differ
by a factorof 16. A "t-like" statistictest (Li 1974),
which accounts for unequal variances between two
groups, indicates that the mean UV-B transmittance
of temperateand arctic species is significantlyhigher
(P < .05) than that of the equatorial and tropical

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616 RONALD ROBBERECHT ET AL. Ecology, Vol. 61, No. 3

EUCALYPTUS, HAWAII ECHEVERIA PERU

.
bc.Oj~~~~~c........~~~~............
.......
80 200. -20

60- -4060 40
0
ABSORPTANCE (0)

40- -60 40 ABSORPTANCE 0m

LUJ
(0/)
-n
20- 80 20 80 r

10 0- -100 O.l
GERANIUM HAWAII ARGYROXIPHIUM, HAWAII >

40--60 4060 40

ABSOR PTANCE (0/)

20- 80 20- 80

0 ....1000
,--,--., . .00 k-
300 320 340 360 380 400 300 320 340 360 380 400

WAVELENGTH(nm)
FIG. 2. Leaf epidermalUV optical propertiesof four species fromexposed habitatsin equatorial and tropicallatitudes.
Three major types of leaf surfacecharacteristicsare represented:(1) glabrous(Eucalyptusglobules), (2) glaucous (Echeveria
sp.), and (3) pubescent (Geranium tridensand Argyroxriphium sandwicense). Althoughattenuationof IJV-B radiationwas
similarlylow in these species, the mannerin whichthe radiationwas attenuateddifferedamong the species. Plant collections
were fromnear the summitof Haleakala, Island of Maui, Hawaii, and fromnear Tarma, Peru. The collection sites were
approximately3000 m in elevation. Reflectanceand transmittanceare representedby stipplingand solid areas, respectively.

species. The temperate-latitude species exhibitedthe previous year's crop. The latter cultivationpractice
greatest range in magnitudein epidermal UV trans- could result in a certain degree of genetic change in
mittance.These species were not collected froman these plants.
alpine vegetation zone, but rather representherba- Four species, differingin leaf surface characteris-
ceous vegetationin eithera Pseudotsuga-Populus or tics, illustratehow epidermalUV-B attenuationis par-
Acer grandidentatumzone, at approximately1700 m titionedbetween reflectanceand absorptance in dif-
elevation. Over the 290 to 400 nmwaveband, the spec- ferentspecies (Fig. 2). The species were collected
tral distributionof epidermalUV transmittancetends fromexposed habitatsin high-elevationtropicalmoun-
to be a species characteristicand appears to be con- tains. Althoughless than 1% of the incident UV-B
sistent under differentenvironmentalconditions. In radiationfluxpenetratesto the mesophylllayerin each
contrast,epidermaltransmittancecan vary in magni- ofthese species, the proportionreflectedand absorbed
tude (Robberecht,personal observation). varies considerablyamong these species. For exam-
A certaindegree of phenotypicplasticityin epider- ple, UV-B reflectancewas 5% forglabrousEucalyptus
mal UV-B transmittancewas foundin Pisum sativum leaves (fromtreesintroducedfromAustralia),approx-
'Alderman'. Epidermal transmittance significantly imately 20W for glaucous Echeveria and pubescent
(P < .05) decreased in response to UV-B irradiation leaves of Geranium,and 40W forpubescent leaves of
undergreenhouseconditions,althoughit was stillnot Argyroxiphium. The epidermalhairs were moredense
as low as thatof plants in the fieldenvironmentin the on Argyroxiphium leaves than on those of Geranium.
Andes. An interpretation of this discrepancybetween Less than 5% UV-B was reflectedfrom pubescent
epidermal transmittanceof field- and greenhouse- leaves of Espeletia schultzii.
grown plants is difficultbecause the environmental
DISCUSSION
conditionsduringcultivationsubstantiallydifferedbe-
tween greenhouse and field habitats. Furthermore, A considerablerangein incidentsolar UV radiation
thereare uncertaintiesabout the seed source and ge- exists along a latitudinalgradient.This is the resultof
neticcompositionof the Pisum plantsexaminedin the a natural gradient in thickness of the stratospheric
Andes. Peruvian farmersgenerallypurchase new Pi- ozone layer, prevailingsolar angles, elevation above
sum seed each season (Moreno, personal communi- sea level, and an optical amplificationeffect(Caldwell
cation), althoughsome farmersmay use seed fromthe et al. 1980). At theirseasonal solar radiationmaxima

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June 1980 LEAF UV OPTICAL PROPERTIES 617

elevations in the tropics,the incidentUV-B radiation

on a daily basis mightbe reduced by 40%, but this
60 NO UV-Bv/ formof avoidance is less effectivethan absorptionof
the radiation in epidermal tissues. Among the plant
LOGAN,UTAH/ / species surveyed in this study, there is no apparent
g 50 (GREENHOUSE-GROWN) / /
latitudinalgradientin prevailingleaf orientation.Thus,
thisformof radiationavoidance does not appear to be
0 40 /UV-B of particularsignificance,as we see it now.
Z/
Attenuationof UV-B radiationin outer leaf tissues
constitutesa major formof adaptationforthe protec-
tion of sensitivephysiologicaltargetssuch as chloro-
z
plasts fromUV-B-induced injury. Optical properties
F 20
(reflectanceand absorptance) thataffectthe radiation
path differin relative importancein differentspecies
10 (see Fig. 2). Reflectanceis influencedby leaf surface
HUANCAYO, PERU
(FIELD-GROWN) characteristicssuch as epidermalhairs or wax depos-
its. A glaucous coating on the leaf may increase re-
300 320 340 360 380 400 flectance,as in the case of Echeveria sp. (Fig. 2), or
WAVELENGTH (nm) Dudleya brittoniiJohansen (Mulroy 1979). Similarly
FIG. 3. Epidermal transmittanceof Pisum sativum 'Al- high UV reflectancemay also resultfromleaf pubes-
derman' under three UV-B radiationflux rates. The plants cence, e.g., Argyroxiphium sandwicense. A pubescent
at Logan, Utah, were grownand UV-B irradiatedin a green- or glaucous leaf surface,however, is not necessarily
house. The UV-B fluxrate was 0 or 2100 biologicallyeffec-
tive J m-2 d-1. The Peruvian plants were field grown and indicativeof highUV reflectance.Althoughthe
dense-
received up to 2700 biologicallyeffectiveJ m-2 d-1. In the ly pubescentleaves of Espeletia schultziireflectabout
greenhouse, the UV-B irradiatedplants exhibited a signifi- 15% of the visible portion of the spectrum(Baruch
cant decrease in epidermaltransmittance(P < .05). 1975), UV-B reflectanceis even lower, at no more
than5% (Darling,personal communication).Such low
UV-B reflectancemay result fromthe absorption of
UV by certain flavonoid compounds located on the
the equatorial and arctic research sites differedin in- epidermalhairs, by a mechanismsimilarto thatdem-
tegrateddaily UV-B irradianceby more than seven- onstrated for epidermal papillae of flower petals
fold,on a DNA-effectivebasis. Equatorial and tropical (Brehm and Krell 1975). Althoughcertain pubescent
species are exposed to the most intense UV-B radia- or glaucous leaf surfacesappear to be effectiveat re-
tion flux along the gradientand, correspondingly,as flectinga substantial portion of the incident UV-B
a group exhibitedthe most effectiveepidermalatten- flux, these representratherspecialized and atypical
uation of radiation (Fig. 1). Furthermore,epidermal surfaceadaptationsofalpine and arctictundraspecies.
UV-B transmittance was consistentlylow amongthese In general, ultravioletreflectancefromglabrous leaf
species, as evidenced by the low variationin the mag- surfaces(e.g., Eucalyptus globules) is low (Gausman
nitudeof transmittanceamong these species (Fig. 1). et al. 1975). Absorptance of UV in the epidermisis
Althoughplantsat these low-latitudesites are exposed usually more importantin effectingthe low transmit-
to a substantiallygreater UV-B radiation flux than tance.
those at higherlatitudes,the calculated effectiveUV- Flavonoids and relatedphenolic compounds consti-
B irradianceat the mesophyll(Imes)is not significantly tuteimportantcomponentsof the UV-B absorptionin
different fromspecies in the temperatelatitudes(Fig. plantepidermaltissues. These pigmentsexhibitstrong
1). This suggests that the epidermis of low-latitude UV absorptanceand yet are largelytransparentin the
species is more effectivein attenuatingincidentUV- visible portionof the solar spectrum(Goodwin 1976,
B radiation,and an apparentlatitudinaltrendof mean McClure 1976, Seigler 1977). High concentrationsof
epidermalUV attenuationeffectively compensatesfor these UV-absorbingpigmentsmay partlyexplain the
the pronouncedgradientof biologicallyeffectivesolar consistentlylow UV transmittancein equatorial and
UV-B flux.A low level of Imesis thusmaintainedalong tropical species. Alkaloids also exhibit appreciable
the gradient. absorption in the UV-B spectrum. Levin (1976) has
The UV-B radiation flux to which plants are ex- presented a convincingnegative correlationof alka-
posed along this latitudinalgradientis representedas loid-bearingplant species with latitude. Species that
that incidentupon a horizontalplane (Fig. 1). Leaf possess alkaloids are proportionatelytwice as preva-
inclinationis not as effectivein reducingincidentUV- lent in tropicalflorasas in the florasof temperatelat-
B radiation as is the case for total solar radiation itudes. Moody (1977) has furthershown that floras
(Caldwell et al. 1980). In certain cases, such as high whichdo not appear to fitthis latitudinalgradientcan

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618 RONALD ROBBERECHT
be broughtinto line by accountingfor tectonic plate
movementsin the last 50 millionyr. Althoughthe se-
lective advantage of alkaloids has primarilybeen at-
tributedto a defensive role against herbivores,alka-
loids in plantleaves may also functionas filtersof UV
radiation.
Changes in UV-absorbingpigmentswithinthe epi-
dermal tissue layer may explain a portionof the UV-
B acclimationof plants when grownunder intensified
UV-radiation (Fig. 3 and Robberecht and Caldwell
1978). The studies by Robberechtand Caldwell (1978)
and Bogenriederand Klein (1977) suggest that some
degree of phenotypic plasticity in the response of
plants to UV radiationexists. The formerstudydem-
onstratedthat plant species can acclimate to UV-B
radiationand reduce theirsensitivityto thisradiation.
Biosynthesisof certainflavonoidscan be specifically
induced by UV-radiation (Wellmann 1974), although
other environmentalfactors also influenceflavonoid
composition in plant tissues (McClure 1976). This
mechanismmay explain the increased UV attenuation
found in some species exposed to UV irradiation
(Robberechtand Caldwell 1978). Increased epidermal
attenuationof UV-B radiationresultsin a lower Imes'
and could therebyreduce the sensitivityof a species
to UV-induced injury(see Fig. 3).
Species havinga highdegree of phenotypicplastic-
ity, i.e., the capability to adjust epidermal transmit-
tance and thereby maintain a low ImeS, might be able
to acclimatize to highUV-B irradianceenvironments.
This may be a partial explanation for the successful
introductionof temperate-latitude agronomic species
such as Viciafaba and Pistin sativumintohighmoun-
tainvalleys of the PeruvianAndes. Furthermore,such
acclimatizationin epidermal transmittancealso may
have occurred in several wildland species of temper-
ate-latitudeorigin that have invaded equatorial and
tropical regions where the natural UV-radiationflux
is substantiallyhigher(see Table 1).
Other adaptations to a high UV-B radiation flux,
such as more efficientrepair systems (Smith 1978),
may also play a role in such an accommodation of
higherUV-B fluxenvironments.The degree to which
phenotypicplasticityor genetically-basedchanges in
plantpopulationsare involvedin plantacclimatization
remainsan open question.
ACKNOWLEDGMENTS
This research was supportedby grantsfromthe National
ScienceFoundation(DEB-7622381)and theNationalAero-
nauticsandSpace Administration Wegreatly
(NAS-9-14871).
appreciatethe assistance of manyindividualson thisproject:
J. Lanat of the Huancayo Observatory,Peru, for providing
technicalassistance and facilities;I. Dirmhirnof Utah State
Universityfortechnicalassistance in designingthe integrat-
ing sphere; M. Darling of Duke Universityfor assistance in
preliminarystudies; U. Moreno and C. L6pez-Ocafia of the
Universidad Nacional Agraria in Peru and Z. Baruch of the
UniversidadSimon Bolivar in Venezuela forcoordinationof
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All use subject to JSTOR Terms and Conditions
ET AL. Ecology, Vol. 61, No. 3
fieldstudies in South America; C. Smithof the Universityof
Hawaii and the National Park Service forarrangementsand
provision of facilitiesfor work in Hawaii; G. Laursen and
the Naval Arctic Research Laboratory at Barrow, Alaska,
forcooperationand fieldfacilities;J. Mulroyand S. Billings
forfieldassistance.
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