BotanicalJournal of the Linnean Socieg (1981), 83: 57-84. With 24 figures
Pigment distribution, light reflection and cell
structure in petals
Q. 0. N. KAY, H. S. DAOUD
Department of Botany and Microbiology, University College, Swansea SA2 8PP
AND
c. H. STIRTON
Botanical Research Institute, Private Bag X I O I , Pretoria 0001, South Africa
Accepted for publuatwn September 1980
Petal structure and the distribution of pigments in petals were studied in relation to the functional
anatomy of petals and the ways in which petals absorb and reflect light. We examined 201 species from
60 angiosperm families. Anthocyanins, betalains and ultraviolet-absorbing flavonoids were normally
confined to the epidermal cells, occurring in solution in the vacuole; carotenoids were found in the
epidermis and in smaller quantities in the mesophyll, normally in chromoplasts. I n a few species,
mainly blue-flowered members of the Boraginaceae and Liliaceae-Scilleae, anthocyanins were
confined to the mesophyll.
Six basic kinds of petal epidermis anatomy were found, sometimes in combination; papillate ( 1 12
species) and multiple-papillate (13 species), in which the conical-papillate form of the cells traps
incident light and scatters emergent light, with surface striations aiding these functions in many cases;
reversed-papillate (4 species), multiple reversed-papillate (29 species), lenticular (32 species) and flat
( I 1 species), all with surfacestriations in some cases. Light is usually reflected from petals mainly by an
aerenchymatous unpigmented reflective mesophyll; in certain species this is replaced by a reflective
layer of starch grains in the upper mesophyll.
KEY WORDS:-flavonoids
-
papillae
-
petal structure - pigments - striations.
CONTENTS
Introduction . . . . . . . . .
Materials and methods.
. . . . . .
Results and discussion . . . . . . .
Petal pigments
. . . . . . .
Structure and function of the petal epidermis
Reflection and absorption of light by petals.
Optical properties of papillate cells.
. .
Optical functions ofstriations . . . .
Structure and function of petal mesophyll .
General discussion. . . . . . .
References.
. . . . . . . . .
0024-4074/050057
+ 28 $02.00/0
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . .
. . .
. . .
. . .
. . .
. . .
. . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . . .
. . . .
. . . .
. . . .
. . . .
. . . .
. . . .
. . . .
. . . .
.
.
.
.
.
.
.
.
.
.
.
58
59
59
59
60
63
76
79
80
82
83
51
0 1981 The Linnean Society of London
58
Q. 0.N. KAY ET AL.
INTRODUCTION
The chemistry, biochemistry and taxonomic distribution of petal pigments have
been intensively studied for many years, and an immense and increasing body of
data has been amassed on these topics (Harborne 1967, 1975, 1977). There
remains a surprising lack of data on the distribution of these pigments within the
cells and tissues of living petals; indeed little is known of the range of cell structure
in the petals of angiosperms. There is a corresponding lack of understanding of the
relationships between petal structure and pigment distribution, and of the ways in
which petals absorb and reflect light and thus acquire their characteristic colours,
brightness and textures. Little progress has been made in this field since the work of
Exner & Exner (1910), who investigated the relationships between petal
structure and function in a common kind of petal with a conical-papillate,
pigment-containing epidermis above an aerenchymatous mesophyll, and also
investigated the less common Ranunculus kind of petal. Their conclusions, which are
discussed below, were largely correct but were limited to certain aspects of petal
function and structure. Exner & Exner’s work is surprisingly little-known today.
The remarkable and distinctive surface structures of the outer cell walls of the
epidermis of petals have recently been investigated with the SEM in major plant
families such as the Asteraceae (Baagrae, 1977a, b, 1978), Fabaceae (Stirton, 1980),
Orchidaceae (Ehler, 1976) and Asclepiadaceae (Ehler, 1975). An attempt has also
been made to establish a universal terminology for describing the different types
and patterns ofsurfaces found in petals, leaves and seeds (Barthlott & Ehler, 1977).
However, there have been few recent studies of the internal structure of petals, and
there appears to be little discussion on the mechanisms by which petals reflect light
whether externally or internally. Although the functions and general features of
the two main kinds of reflective tissue in petals were correctly described by Exner
& Exner in 1910, their work has been forgotten and is ignored in recent
publications concerned with the reflective properties of petals (e.g. Stickland,
1974; Kevan, 1978).
Observations that anthocyanins are confined to the epidermis of the petals are
scattered through the literature (e.g. Hildebrand, 1863; Blank, 1947; Arditti &
Fisch, 1977). A smaller number of workers has observed that this was also true for
ultraviolet-absorbing flavonoids (Caldwell, 1971; Stewart, Norris & Asen, 1975;
Arditti & Fisch, 1977) and in some instances for carotenoids (Paech, 1955; Arditti
& Fisch, 1977). The published data are sufficient to justify assertions of the kind
made by Exner & Exner (1910) that petal anthocyanins are known to be localized
in the epidermis.
There are similarly scattered observations of the occurrence of petal epidermises
with a conical-papillate cell structure (e.g. Muller, 1893; Exner & Exner, 1910;
Parkin, 1928; Knoll, 1938; Stewart et al. 1975; Roberts & Humphreys, 1980) but
published data on the nature and distribution of this type of epidermis are sparse.
Apparently the best source of published information on the structure of the petal
epidermis is the survey made by Schubert (1925), who investigated more than 330
species from 51 families and gave some data on pigment distribution in the petals of
120 species. Schubert was mainly concerned with the gross morphology of the petal
epidermis, especially the occurrence of papillate cells. He hardly commented on
surface striations, and his observations of pigment distribution were confined to
visible pigments in 30 families; he made few observations of the internal structure
FUNCTIONAL ANATOMY OF PETALS
59
of petals and failed to obtain satisfactory petal sections for many species. We have
investigated pigment distribution and petal structure in 201 species from 60
angiosperm families, including 41 of the families studied by Schubert (1925).
MATERIALS AND METHODS
Fresh, fully-open flowers were obtained from wild plants or cultivated plants of
known origin. Standard methods of fixation and preparation (Hall, Skerret &
Thomas, 1978; Daoud, 1980) were used for all work with the SEM, but fresh
unfixed petals were used in all other investigations, either unmounted, or mounted
in water. Fresh petal sections were cut by hand with a sharp razor blade and
examined immediately. Ultraviolet microphotographs were made by transmitted
light with a Schott UG1 or UG5 filter inserted into the optical system of the
microscope to exclude visible wavelengths ; a high-temperature electronic flash
provided the source of ultraviolet light, and Kodak Tri-X or Ilford FP4 film was
used (Daoud, 1980). The localization of ultraviolet-absorbing pigments in the
petal was determined either by ultraviolet microphotography of fresh sections, or
by irrigating fresh sections mounted in water with ammonium hydroxide solution;
most flavones and flavonols then become visible as yellow pigments, because their
absorption spectra are shifted bathochromically in alkaline solutions. In several
cases the ultraviolet-absorbing pigments were also extracted and isolated by
chromatography, and provisionally identified by ultraviolet spectroscopy with a
Unicam 8000 recording spectrophotometer, using standard techniques (Mabry,
Markam & Thomas, 1970; Daoud, 1980).
RESULTS AND DISCUSSION
Petal pigments
Our data for the distribution of petal pigments are compared with the data of
Schubert (1925) in Table 1 and summarized in Table 2. Our results show that, in
the wide range of families investigated, both anthocyanins and ultravioletabsorbing flavonoids appear to be substantially confined to the epidermis in the
majority of petals. However, there are certain exceptions to this general rule,
notably blue-flowered members of the Boraginaceae and Liliaceae-Scilleae in
which the blue anthocyanin pigments occur mainly or entirely in the mesophyll.
We have also observed that anthocyanins, yellow flavones and flavonols, and the
ultraviolet-absorbing flavones and flavonols of ‘white’ (insect-yellow ; Kay, 1979)
petals normally appear to be present in solution, evenly dispersed through the
vacuoles of the epidermal cells, and are rapidly lost from damaged and marginal
cells in preparations mounted in water (Figs 1-4). This is probably also true of
ultraviolet-absorbing flavonoids in carotenoid-containing epidermal cells (Daoud,
1980). We have not observed any apical concentrations of ultraviolet-absorbing
pigment granules in living cells of the type reported in the papillate epidermis of
freeze-dried petals by Brehm & Krell (1975). These could have been artefacts
produced during the process of freeze-drying, in the manner discussed by Hall, et
al. (1978).
60
Q. 0.N. KAY ET AL.
Figures 1-4. Sections and surface views of fresh petals mounted in water, showing the shape of the
papillate epidermal cells and the restriction of water-soluble ultraviolet-absorbing compounds to the
epidermal cells. Fig. 1 SuxiJrugu rosuceu, in visible light, longitudinal section, x 150. Fig. 2. Suxifrgo
rosuccu in ultraviolet light of 33(t400 tun, x 150. Fig. 3. Lnrcanthcrnum vulgure, in visible light, edge of
lamina showing surface and side views of papillate cells of upper epidermis, x 210. Fig. 4. Lcucunthrmum
vulgure, in ultraviolet light of 330-400 nm, x 210.
Structure and functions of the petal epidermis
Although the data of Schubert (1925) on the shape of the outer cell walls of the
petal epidermis are extensive, he gave little information on the occurrence of
surface striations on the outer cell wall, and his observations of the shape of the
inner cell wall are of uneven quality. Of the 201 species examined by us (Table 2),
45 had been investigated (or were closely related to species investigated) by
Schubert. Although our results generally agree, the occasional shortcomings of his
observations are clear. His failure to observe any of the many cases in which the
epidermal cells are multiple-papillate is particularly striking. Multiple-papillate
cells (which do not appear to have been reported previously) are longitudinally
elongated, and may bear a row of acute papillae on the outer face with a
corresponding row of lenticular projections on the inner face, as in many
Caryophyllaceae and Cistaceae (Figs 5-8), or may have a row of lenticular
projections on both faces, as in Anagallis amensis (Figs 7,8), or may have a relatively
flat outer face with a row of lenticular or papillate projections on the inner face
FUNCTIONAL ANATOMY OF PETALS
61
(reversed multiple-papillate) as in Crocus species and some Caryophyllaceae and
Papaveraceae (Figs 9, 10). Schubert’s failure to observe cells of any of these
multiple-papillate kinds may have been the result of his reliance on transverse
sections; in order to observe multiple-papillate cells, which are normally of
considerable length, one must prepare longitudinal sections of the petal because in
transverse sections the multiple-papillate cells are cut and consequently collapse.
Figures 5-10. Longitudinal sections (Figs 5, 7, 9) and surface views (Figs 6, 8, 10) of fresh petals
mounted in water, showing multiple-papillate and reversed multiple-papillate epidermal cells. Figs 5,
6. Cisfus albidus, x 420 (acute multiple-papillate). Figs 7,8. Anugalks arumrb, x 480 (rounded multiplepapillate). Figs 9, 10. Pupavn dubiwn, x 420 (reversed multiple-papillate).
Q. 0.N. KAY E l AL.
62
Schubert observed and figured a very large number of cases in which the petal
epidermis was of the common, singly conical-papillate kind, as in Viola (Fig. 6),
and he discussed extensively the possible relationships between structure and
function in this kind of epidermis. His view that the papillae functioned as
footholds for pollinating insects in certain specialized cases (e.g. Convallaria mujulis
and Pobgonatum species) may be correct. His dismissal of the theory of Hiller (1884)
that the petal epidermis functioned as a water-storage tissue is convincing, but his
own conclusion that the major function of the papillate epidermis was to act as an
energy-concentrating light-absorbing tissue, in which metabolism was enhanced as
a result of increased temperature, has little evidence to support it. A similar
function had already been proposed for the papillate epidermises of some shadeleaves (Solereder, 1908; Haberlandt, 1914). Papillate epidermises also occur in
secretory organs (including floral nectaries) and on the receptive surface of the
stigma, but it is clear that the functions of these papillate epidermises differ from
those of the surfaces of petals, although secretory cells may sometimes occur on the
petal lamina (Loomis & Croteau, 1973). The surface morphology of the petal
epidermis may also act directly as a specific tactile or visual recognition stimulus in
certain cases, as Kullenberg (1961) has suggested for Obhrys and Stirton (1980) for
Fabaceae. The papillate epidermis of the petals of Rosa species may aid flower
opening (A. V. Roberts, personal communication) ; in the light of this suggestion it
seems that the concertina-like structure of the multiple-papillate petal epidermises
of Cistaceae and Papaveraceae may aid the rapid petal expansion that is
characteristic of these families, while similar multiple-papillate or multiple
reversed-papillate petal epidermises in other families may function in a similar way
during diurnal opening and closing, as for example in Anagallis, many
Caryophyllaceae-Alsinoideae, Crocus and Oenotheru (Table 2). Our observations
strongly support the conclusion of Exner & Exner (1910) that the primary function
of the papillate epidermis of petals is to act as a light-trap for incident light and, in
conjunction with the reflective mesophyll, to guide incident light through the
pigments contained in the epidermal cells and to return it to the exterior by a
combination of external reflection, refraction and internal reflection.
Schubert
Present survey
Anthocyanin Carotenoid Anthocyanin Carotenoid UV-absorbing pigment
Substantially confined
to epidermis
64 (21)
20 ( 1 1 )
73 (38)
10 (7)
83 (34)
Also clearly present in
some mesophyll cells
-
20 ( 1 1 )
8 (7)
20 (16)
24 (18)
10 (5)
5 (3)
8 (3)
-
-
Mainly or exclusively
in mesophyll
FUNCTIONAL ANATOMY OF PETALS
63
Figures 11, 12. Petals of Viola tricolor. Fig. 11. Longitudinal section, x 510, mounted in water, showing
the shape of the conical-papillate cells of the upp& epidermis and the epidermal localization of
pigment. Fig. 12. Petal surface, x 160 in incident light, showing the surface reflections from the tips of
the conical-papillate cells of the upper epidermis.
Rejlection and absorption of light by petals
A typical papillate petal epidermis absorbs incident light very efficiently, in that
almost all incident light enters the epidermal cells, with only a small proportion
being reflected directly from the outer walls of the papillae towards an observer.
Direct surface reflection is usually confined to the tips of the papillae, which thus
appear as bright spots in photographs of petal surface made by incident light (Fig.
12), especially when a filter which transmits only within the absorption range of
the petal pigment is placed over the camera lens (Knoll, 1938). In contrast,
smooth-surfaced petals, including those of Crocus species and others of the reversed
multiple-papillate kind show strong surface reflections in such photographs (Figs
13--15).The reflectance spectra of papillate petals are noteworthy for their strong
absorption within the absorption range of the petal pigments, again showing that
Figures 13, 14. Flowers of Crocus siebni var. sieberi, xO.8. Fig. 13. I n visible light. Fig. 14. In
ultraviolet light of 330-400 nm (Kay, 1979). The petals (perianth segments) contain an ultravioletabsorbing flavonoid in the epidermal cells; Fig. 14 shows the strong surface reflections from the flat
outer faces of the reversed multiple-papillate cells of the upper epidermis.
DICOTYLEDONS
Apiaceae
Anfhrircw yluestrir (L.) H o f h .
Daucus cam& L.
Heraclnun sp0"dylium L.
Ocnanthe crocah L.
Apocynaceae
Alhmanda catharfica L.
Vinca major L.
Taxon
i
++
++ ++
pq
Pigments in
epidermis
+
++
+ ++
++
++
++
+
Upper epidermis
++
++
++
++
Pigments in
mesophyll
+
+
+
+
+
++
++
++
++
++
Lower epidermis
+
+
+
+
Table 2. Petal structure and pigment localization in 201 species from 60 families. Pigments (anthocyanins, ultraviolet-absorbing flavones,
flavonols or similar compounds ; carotenoids ; or betalains) are completely or almost completely confined to the epidermal cells unless
otherwise indicated. UV-absorbing pigments were probably under-recorded in cells containing anthocyanins. The descriptions of shape of
epidermal cells refer to the outer faces of the epidermal cells, except in the case of the convex-lenticular base which refers to the inner faces
(towards the mesophyll). Examples are figured as follows: papillate, Figs 1, 2, 6 & 13; lenticular, Fig. 10; multiple-papillate, Figs 3 & 4;
multiple reversed-papillate, Figs 5 & 14; convex-lenticular base, Figs 6 & 13; striations on outer cell-wall, Figs 10 & 11. A reflective
mesophyll with air-containing intercellular spaces is present in all cases except Erica tetralix, Anemone species and Rununculusfiaria
Asteraceae
Chamornilla recufifa (L.) Rauschert
Ch:hrysanfht=mumcoronarium L.
I.eontodon hipidus L.’
I a u a n t h u m uulgare Lam.
Mafricaria perjorafa Mtrat
Semcio cruenfus DC.
Berberidaceae
Berberis S P . ~
Bignoniaceae
Catalpa bignonioides Walt.
Incarnillea dclauayi Bureau & Franch.
Boroginaceae
Arnebia rchioides A. DC.
Borago ofiinalis L.
Erhiwn vulgare L.
Lithospmum ofiinalc L.3
Mollkia pefraea (Tratt.) Griseb.
Myosofis arvemis (L.) Hill
M . secunda A. Murray
Brassicaceae
Arabidopsis thaliana (L.) Heynh.
.4rabis caucasica Schlecht.
A. hirsuta (L.) Scop.
Capsella bursa-pashis (L.) Medicus
Cochlearia anglica L.
Erophila VCTM(L.) Chevall.
Aubricta dehidea (L.) DC.
Brassica oleracea L. cv. ‘Continuity’ (white)‘
CardatninepCxuosa With .
C. pratemis L.
Cheiranfhus cheiri L.5 (yellow)s
Raphanus raphanistrum L. (white)‘
Sinapis arvenris L.“
Buddlejaceae
Buddleja dauidii Franchet
Caprifoliaceae
Lonicera perulymenum L.’
Sambucus nigra L.
Viburnum opulus L.
++
+
+
+
++
++
++
++
++
++
++
++
++
++
++
++
++
++
++
++
+
+ ++
++
++
+ ++
++
++
++
++
++
++
++
++
++
++
++
+
+
++
++
++
++
++
++
++
++
++
++
++
++ +
+
+
+
-4-
++
+
++
++
++
++
+
+
+
++
+
+
+
+
+
+
+
+
+
+
+
+ +
+
+
+
+
+
+
+
+
+
+
+
+
++
+
++
++
++
+
++
++
++
++
++
++
++
++
+
+
+
+
++
++
++
++
++
++
++
++
++
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+++++
+ + +
+++++
+
+ +
+
+++ ++ + +++++
+
+++ ++ + +++++
Anthocyanin
UV-absorbing flavone,
flavonol or similar cpd.
gg
G-.
G;'
Carotenoid
Anthocyanin
+
UV-absorbing Bavone,
flavonol or similar cpd.
f
C.
Carotenoid
+
+
+
+:++
+:
+
+
++
++
+
+
+:
+
+
++
++
+++++
+++++
Papillate
Multiple-papillate
Lenticular
++++++
+++++
+++
+++
+
+
+
+
+
?
Multiple-lenticular
Flat
9.
G;'
Multiple reversedpapillate
v)
s
Striations on outer face
n
".
Yapillate
++++
++++
t
Multiple-papillate
CD
e;
Lenticular
Multiple-lenticular
Flat
++++
++++
Convex-lenticular base
+
+
++++ +
C
D
Convex-lenticular base
Reversed-papillate
+:
+++
.
+
++++
+++++
:+
++++
+++
Reversed-papillate
++
s
8
".
D
ti'
Multiple reversedpapillate
Striations on outer face
Celastraceae
Euonymus europaeus L.
Cistaceae
Cistus albidus L.
C. salr>folius L.
Hdianlhmum nummularium ( L .) Millerfi
Convolvulaceae
Ca!ystegia sepium (L.) R. Br.
C.n'lvatica (Kit.) Griseb.
Comaceae
Cornus sunguinea L.
Crassulaceae
Sedum acre L.
S. album L.
Cucurbitaceae
Bryonia dwica L.'
Dipsacaceae
Scabwsa columbaria L.
Sucrisa pratemis Moench
Ericaceae
Erica lptralix L.8
Rhododendron pontuum L.
Gentianaceae
Blackstania perfooliota (L.) Hudson'.
Centaurium erythraea Rafn
Geraniaceae
Erodium cicutarium (L.) L'HCr.
Geranium sanguineum L."
Pelargonium zonale L'HCr.
Gesneriaceae
Saintpaulia ionantha Wendl.
Streplocarpu S P . ~
H ydrangeaceae
Philadelphus coronarius L.
H ypericaceae
Hypericum patulum Thunb.6
H . perfooratum L.6. '
Lamiaceae
Lamium album L.
Rosmarinus of&inalis L.
Saloia p a k m Cav.
++
++
++
++
++
++
++
+
++
++
+
+
4
+-I
++
++
+
++
++
++
++
++
++
++
++
++
++
+ ++
++
++
++
++
+i
+-I
+ ++
++ + +
++
++
t+
++
+
t+
t+
++
t+
++
++
++
++
++
++ +
++
++
t+
++
++
+
++
++
++
+
++
+
++
++
++
++
++
++
++
++
++
++
++
++
++
++
++
++
+
+
++
++
++
++
++
++ +
++ +
+
++
+
+
+
++
++
++
+
+
+
+
+
+
+
+
+
+
+
+
+
+ +++
+ +++
+++ + ; ;
++
++
++ +
++ +
+ +
+
+
Anthocyanin
UV-absorbing flavone,
flavonol or similar cpd.
+ +
++
Carotenoid
gg
$B
&' r.
P
Ant hocyanin
UV-absorbing flavone,
flavonol or similar cpd.
++
++
++
+
+
Carotenoid
+
+
Papillate
Multiple-papillate
;+
+
Lenticular
C
+ +
+ +
-0
2.
Flat
B
Multiple-lenticular
0
B
+
+
Convex-lenticular base
g
6'
Reversed-papillate
++ ++ ++ ++
+++++++ +
+:
+:
+
+
+
+
++ ++ ++
+
Multiple reversedpapillate
Striations on outer face
+
+
(I]
3-
3
4
Papillate
Multiple-papillate
n
c
Lenticular
+
+ I F
+ +
+ +
+
t
0
Flat
9
Multiple-lenticular
Convex-lenticular base
Reversed-papillate
++ ++ ++ ++
+++ +++ +
++
+
+
-54
3
G;'
Multiple reversedpapillate
+
Striations on outer face
v,
Oxalidaceae
Oxalir arficulata Savigny
Papaveraceae
Chelidonium majus L."
Papaver dubium L.
P . somnijium L.S
Paeoniaceae
Paeonia daurua Andrews
Papilionaceae' I
fafus corniculatus L.
Trijolium prafense L.
1.repens L.
Ulex curopaeus L.'
Plurnbaginaceae
Amma marifima (Miller) Willd.
Polernoniaceae
Phlox douglarii Hook.
Polemonium caeruleum L.
Polygonaceae
PoIygonum lapathijolium L.'
Prirnulaceae
Anagallis amensis L.
A . h l l a (L.) L.
Cyclamen persicum Miller
Glaux maritima L.
Lysimachia m o r u m L.'
Primula cv. 'Variabilis'
Primula verb L.
P . vulgaris Hudson
Samolus mlerandi L.
Ranunculaceae
A m o n e heldreichii Gandoger
A . nemorosa L.I2
Caltha palustris L.'
Delphinium mewiesii DC. (petal)
D . mewiexii (sepal)
Eranthis ciluicus Schott6
Ranunculusjcaria L.l2.l 3
R . peltatus Schrank
Trollius europaeus L.6
++
++
++
+
+
+
+
++
++
t+
+
++
++
++
++
++
++ ++
+
++
++
++
+ ++
+ ++
+
++
++
++
++ ++
+ + ++
++
++
++
++
++
++
++
++
++
++ + +
++
++
++
++
+ ++
++
+
++
++
++ ++
++
++ ++
++
+ ++
++ ++
++
++
++
++
++
++
+
++
+
++
++ +
+
++
+
++
++
+
+
+
++
+
+
++ +
+
+
+
+
+
+
I-+
k+
I-+
+
+ +
++ +
++ +
+
+
+
++
+
+
+
++
++
++
++
++
++
+
++
+
++
++
++
++
++
++
++
++
+
++
+
+
+
+
++
+
+
+
4-
++ +
+
+
+
+
+
+
+ +
++ +
+
+
+
+
+
+
a
Ro
+I
+ +
+ +
+
+
+
++++
++++
+
++
+++++
++++
+++++++ ++++
+++
+++
+
+
+
+ +
+ ++ ++ + +
+ ++ ++ + +
+
+
Anthocyanin
UV-absorbing flavone,
flavonol or similar cpd.
Carotenoid
03
8 i
P'
6'
Anthocyanin
+
t
++;
++++ ++++
++++ ++++
+++
+++
+
+
UV-absorbing flavone,
flavonol or similar cpd.
Carotenoid
@
U
Y
-3
Lenticular
+
;;++:++
3 ?.
Papillate
Multiple-papillate
++
Multiple-lenticular
; :;+++++
+
C
U
4
4
Convex-lenticular base
0
Flat
B.
P'
Reversed-papillate
+ ++ ++++ +++++++++++++
+
+
++++
+ ++
;+++
++
++
++
+++
+++
+
I
v,
a-
P
Multiple reversedpapillate
Striations on outer face
%
Ip
z.
R
c3
Papillate
0
Multiple-papillate
+
+
Lenticular
Multiple-lenticular
+++
+++
++
++
Flat
0,
G;
2
0
B.
%
P'
Convex-lenticular base
I
Reversed-papillate
Multiple reversedpapillate
+ +++++++ +++ +++++++++
1 Striations on outer face
Saxifragaceae
Bngenia crassiiolia (L.) Fritsch
Sarijaga cv. 'Brevifolia'
s. granulah L.
S. hypnoides L.
S. rosacea Moench
S. cv. 'Burnatii'
S. cebmnmrti Rouy & Camusg
S. spathularti Brot.
S. hidactylites L.
Scrophulariaceae
Cymbalaria muralti P. Gaertner, B. Meyer & Scherb.
Euphracia rostkoviana Hayne
Hebe sp.
Rhodochiton atrosang;uncUnr (Zucc.) Rothm.
Veronica chamacdys L.
Solanaceae
Cesfmn purpvrm Standl.
Solannm dulcmnnra L.
Tropaeolaceae
Tropacolutn ma& L.
Valerianaceae
Centranthus tuber (L.) DC.
vd&M O&M/k L.
Verbenaceae
Clnodcndon sp.
Verbena ofinalti L.
Violaceae
V w h curtirii E. Forster (yellow)
V. riviniana Reichb.
v. hicolor L.
V. z uritlrockiana Cams
MONOCOTYLEDONS
Alismataceae
A l i m lancmhtwn With.
Amaryllidaceae
Galanthw niualir L.
Nm'ne bowhii W. Watson"
Butomaceae
Butanus umbelhhrr L.
Commelinaceae
Sebmasea purpurea Boom
Tradcscantia virginiana L.
++
++
++
++
+
++
++
++
++
+ ++
++
++
+
++
+
+
++
++
++
++
++
+ ++
++
++
++ +
++
++
++
++
++
++
++
+ ++ +
++
++
+
t+
t+
t+
t+
t+
t+
+
t+
t+
t+
t+
t+
+
t+
t+
+
t+
t+
t+
t+
t+
t+
t+
+
++
++
++
++
+
++
+
+
+
++
++
++
++
++
+
++ t
+ +
t
t
t
t
t
++
+
+
+
+
+ ++
+
t +
+
t
+
++
t
+
t
+
+
+
+
+
+
t +
t
++
+
+
+
++
++
++
++
++
+
++
+
++
+
+
++
+
++
+
+
+
++
++
++
++
++
++
+
+
+
+
++
+
++
+
+
+
+
+
+
+
+ +
++ +
+
+
+
+
+
+
+
+
+
+
+
+
+
+
:;+:
+
++:
+
4-
+:
+++++++
:+
++++++
++ ++ ++ ++ + + ++ ++ ++
+
+
+$+
Anthocyanin
UV-absorbing flavone,
flavonol or similar cpd.
gg
u2=.
D'
II
Carotenoid
Anthocyanin
+ +
UV-absorbing flavone,
flavonol or similar cpd.
++
++
++++
++++
Carotmoid
ULa
.L
F a-.
-3
Papillate
Multiple-papillate
++ ++ ++ ++
Lenticular
C
+
+
+;+
3.
Flat
s
Multiple-lenticular
Convex-lenticular base
U
0
R
G;'
Reversed-papillate
+:
+
+
+
++++++
+++
+++
;+
+ +
++;+
v1
5
5
Multiple reversedpapillate
Striations on outer face
9,
0
3.
B
c
Papillate
Multiple-papillate
+ +
n
0
G;
Lenticular
c
(
Multiple-lenticular
+ ++ +++
+ ++ +++
b
3
Reversed-papillate
+++
+++
+ : ;+
+
++++++
+ +
Multiple reversedpapillate
Striations on outer face
Orchidaceae
Anacmpfu pyramidalis (L.) Rich.
Dacglorhiza futlm'i (Druce) soi,
Zingiberaceae
Roscoea alpina Royle
++
++ ++
++
+
++
++
+
+
++
+
+
++
+
+
+
+
74
Q. 0.N. KAY ET AL.
Figure 15. Petal of Crocur vmurc in visible light, x 160. Note strong surfice reflections from upper
epidermis.
very little light is reflected directly from the outer surface; almost all the light that
is reflected from the petal has passed through the pigments contained within the
epidermal cells.
If the aerenchymatous mesophyll of a typical petal is exposed by stripping off
part of the epidermis, it normally appears white or almost white in colour to the
human eye; it reflects ultraviolet light as well as visible light and is thus insectwhite, in the sense of Kevan (1978) (Figs 16, 17). Its true colour thus differs from
that of normal ‘white’ petals, which with rare exceptions (Kay, 1979) contain
ultraviolet-absorbing pigments, usually flavones or flavonols (Roller, 1956;
Harborne, 1967; Daoud, 1980) in the epidermis (Tables 1, 2) and are thus insectyellow (Kevan, 1978). If the epidermis is stripped from small areas of such
ultraviolet-absorbing ‘white’ (insect yellow) petals to expose the ultravioletreflecting mesophyll (insect white), both parts appear white to the human eye but
contrast very sharply in photographs taken with a filter that transmits ultraviolet
but not visible light (Figs 16, 17). This corresponds to the visible contrast between
the exposed white mesophyll and the intact coloured lamina when part of the
epidermis is stripped from petals with anthocyanin pigmentation (Exner & Exner,
1910).
Optical properties of papillate cells
The data in Table 2 show that there are several different kinds of petal anatomy,
which may represent different adaptive complexes. The most common kind of petal
epidermis is the simple conical-papillate kind, with or without striated outer walls.
The striking, but apparently previously unobserved multiple-papillate kind (Figs
5-10), which we have so far found only in Caryophyllaceae, Cistaceae,
Hypericaceae, Onagraceae and Primulaceae appears to have very similar optical
properties. The inner faces of the papillate epidermal cells are usually convexlenticular in petals with anthocyanin or ultraviolet-absorbing flavonoid pigments
in clear solution, but are often more or less flat in petals containing carotenoid
pigments; the carotenoids normally occur in a basal layer of chromoplasts, with a
FUNCTIONAL ANATOMY OF PETALS
15
Figures 16, 17 Lamina of ray-floret of Lcucanthnrn vulgarc with part of the ultraviolet-absorbingupper
epidermis stripped to reveal the ultraviolet-reflectingrnesophyll, x 10. Fig. 16. In visible light. Fig. 17.
In ultraviolet light of 330-400 nm.
secondary apical group in some cases. The papillate cells range in height and shape
from exceptionally tall and acute papillae like those of Dianthus barbatus, Arnebia
echioides and Primula vulgaris to short stumpy papillae, as in Dryas octopetala and
Brassica oleracea ; the latter are clearly transitional to the lenticular type of
epidermal cell. The shape of the papillate cells varies widely, and the optical
properties associated with different shapes must differ. The most common form of
papillate cell is subconical in form with a rounded apex, slightly concave outer
walls and a somewhat expanded convex base (Figs 1, 2, 11). A distinctive kind of
epidermis is found in the Geraniaceae, in which the papillae are usually low and
wide with strongly concave outer walls and a strongly concave base. Another
unusual kind occurs in some Saxifraga species, in which the tip of the papilla forms
a convex-ended projection, which is cylindrical or even distinctly waisted below.
The range of variation in Saxijraga is unusual in including both species with
smooth outer papilla walls, as is S. cebennensis, S. hypnoides and S. rosacea (all of
which have projecting papilla tips) and species with striated papilla walls, as in S.
spathularis. Within a family it is more usual for the outer cell-walls of the petal
epidermis to be uniformly smooth (as for example in the Caryophyllaceae and
Geraniaceae) or uniformly striated (as in the Asteraceae, Brassicaceae and
Rosaceae). However, the Lamiaceae, Primulaceae, Scrophulariaceae and some
other families include both smooth and striated forms, and further work may show
that both forms of cell-wall occur in families in which only one form has been
reported. The prominence of the striations ranges from weak so that they are only
just detectable, as in Senecio cruentus, to very strong and conspicuous, as in several
Apiaceae and Viola species (Figs 18-21).
A comparison of the optical geometry of a papillate epidermis with that of a flat
epidermis (Fig. 22) shows that a flat epidermis will reflect light that strikes it at a
shallow angle, whereas a papillate epidermis will absorb the light over the greater
part of its surface. Experiments carried out with cell models have confirmed this.
Petals reflect light more or less strongly, but this reflection takes place mainly from
the surfaces of mesophyll cells at cell wall/air interfaces (except in Ranunculus
species and a few similar cases). These processes were described by Exner & Exner
(1910), but they did not consider the optical effects produced by the bases of the
76
Q. 0.N. KAY E l AL.
Figures 18-21. SEM surface views of the upper epidermis of petals, showing typical patterns of
striations on lenticular cells (Figs 18 & 19) and papillate cells (Figs 20 & 21). Fig. 18. P r u w spinosa,
x400. Fig. 19. Scilla bfolia, ~ 5 1 0 Fig.
.
20. Vnonua chamacdvs ~ 4 0 0 .Fig. 21. Dacglorhka fuchsii,
x 600.
papilla cells, nor did they consider the optical geometry of the mesophyll, and they
were apparently unaware of the existence of reversed-papillate and multiplepapillate petal epidermis cells.
If one considers the influence of reflection and refraction in conical-papillate
epidermal cells on reflected light emerging from the mesophyll (Fig. 23), it is clear
that the convex base (if present) will refract this light and that the converging
outer cell walls will reflect it. In this way the light will pass through a more uniform
length of pigment-containing solution than would be the case in flat epidermal
cells. Furthermore, the loss of emergent light by surface reflection from the base of
the epidermis directing it back into the mesophyll will be reduced by the action of
the convex base (Fig. 23). The same mechanisms will scatter the light that emerges
from papillate petals, so that the effects of unidirectional light sources (e.g.
sunlight) are reduced and the brightness of ,the petal remains relatively constant
irrespective of the angle from which it is viewed. Goniophotometric measurements
of the light reflected from different kinds of petal and experiments with detached
epidermises and with cell models have confirmed this. These measurements and
observations have also shown that internal reflection to the exterior from the
convex base of the papilla is only a minor effect in typical conical-papillate
FUNCTIONAL ANATOMY OF PETALS
Figure 22. Light absorption and reflection by a papillate petal surface (left) and a flat petal surface
(right).
epidermises, but is much more important in reversed-papillate and reversed
multiple-papillate epidermises, in which the internal papillae directed towards the
mesophyll correspond to the convex base of a normal papilla (Fig. 24). Reversedpapillate epidermises appear to differ from normal papillate epidermises in a
number of optical features and produce strikingly different optical effects which
can be seen most clearly when (as is the case in many Caryophyllaceae) the two
kinds occur in different areas of the same petal and contribute to petal patterning.
In a simple reversed-papillate epidermal cell, the outer face is relatively weakly
convex but the inner face is semi-ovoid or rounded-conical, so that the cell
resembles a normal papillate cell, but with the papilla facing inwards towards the
mesophyll instead of outwards. Schubert (1925) found this kind of anatomy in
several Verbascum species; we have also found it in Campanula and Roscoea. The
optical properties of a simple reversed-papillate petal epidermis are similar to those
of the much more frequent multiple reversed-papillate kind ; fairly strong surface
reflections from the relatively flat outer face (e.g. in Campanula, Crocus, Papaver,
Tulipa and Verbascum; F'igs 13-15) are common in both kinds and may be
adaptive. The papillate inner face of the epidermal cell will act as a light-trap both
for light reflected from the mesophyll and for light transmitted from below, and it
will also reflect some externally incident light by total internal reflection, in all
cases guiding the light through the pigment contained within the cell.
In the lenticular kind of petal anatomy, the outer faces of the epidermal cells,
and often also the inner faces, are convex. In some respects this kind of petal
anatomy is intermediate between the papillate and reversed-papillate kinds, and
sometimes, as in Campanula, lenticular epidermises lacking striations intergrade
with the reversed-papillate kind. However, lenticular epidermises are more
commonly associated with the normal papillate kind, either forming the lower
epidermis on petals with a papillate upper epidermis, or forming the inner part of a
mainly papillate upper epidermis. Lenticular cells also fairly commonly form the
whole of the upper or both petal surfaces (Tables 2, 3).
Optical functions of striations
The optical geometry of a smooth lenticular petal surface does not enable it to
function as a light-trap, and smooth (unstriated) lenticular petal surfaces usually
show fairly strong surface reflections, as in Campanula rotundifolia and Malva
78
Q. 0.N. KAY ET AL.
Figure 23. Paths of light rays emerging from the reflective mesophyll of a petal with conical-papillate
epidermal cells with convex bases. (A refractive index of 1.35 is assumed; the intercellular spaces in the
mesophyll are air-filled.)
sylvestris. Lenticular cell models also show this effect. Lenticular petal surfaces with
striations on the outer cell walls contrastingly show much weaker surface
reflections (e.g. Cyclamen persicum, Hebe species, Philadelphus coronarius, Sambucus
nigra) and we consider that an important optical function of the striations is to act
as a light-trapping structure; on lenticular epidermises, where they are often
strongly developed (Figs 18, 19) they compensate to some extent for the absence of
light-trapping papillae, and on papillate epidermises they supplement the lighttrapping action of the papillae; in both cases acting in the same manner as the
papilla (reflection and refraction followed by internal reflection (Fig. 22). The
striations on the side-walls of papillae normally run from base to apex (Figs 20,2 l ) ,
thus giving a greater efficiency of light absorption than would be the case for
latitudinal striations. In some species of Galium (as in Galium aparine, G . cruciatwn
and G.verum; Table 2) striations are replaced by small regularly arranged domed
projections of the outer cell-wall,. resembling a miniature version of a papillate
petal epidermis. In Galium aparine the upper petal epidermis is thus doubly
papillate, with papillate cells the outer walls of which are themselves minutely
papillate.
FUNTIONAL ANATOMY O F PETALS
79
Figure 24. Internal reflection of light falling vertically on a multiple reversed-papillate epidermal cell.
The cell is assumed to have a uniform refractive index of 1.35,with the intercellular spaces completely
of vertically incident light will be reflected by this mechanism in cells of this
air-filled. More than 60”,,
basal configuration under these conditions, but the amount of light that is reflected by this mechanism
decreases rapidly as the angle of incidence diverges from the vertical.
A second probable optical function of striations is to scatter emergent light, thus
further increasing the constancy of petal brightness (when viewed from a distance)
regardless of the direction of viewing and the angle of incident light (see above).
However, they may also guide emergent light to some extent, and the possibility
that insects may react to the fine patterning or other optical effects produced by the
striations should be borne in mind and investigated further. Longitudinal
striations, orientated towards the base of the petal, are fairly common (such
striations occur in Oenothera species, Ornithogalum umbellatum, Setcreasea purpurea and
Trfolium repens, for example). The striations do not appear to be capable of
producing any structural colour effects (Daoud 1980).
Structure and function of petal mesopLyl1
The reflective mesophyll cells that are associated with multiple reversedpapillate petal epidermis cells are usually extremely regular in structure, usually
being elongated four-faced cells with a row of small evenly spaced projections
(resembling small papillae) on each face, one face being directed towards the
upper and another towards the lower epidermis. Projections from adjacent cells
meet at their tips, and the intercellular spaces are air-filled. In the
Caryophyllaceae and Cistaceae the mesophyll is composed of two to six layers of
such cells in the examples we have investigated, but three or four layers are most
80
Q. 0.N. KAY ET AL.
Table 3. Cell shape and outer cell wall structure in the upper petal epidermis of
201 species from 60 families. A few species combine more than one kind of
anatomy. The number of families in each category is shown in parentheses
Cell shape
Outer cell wall structure
Striated
Smooth
Papillate
Multiple-papillate
Lenticular
Multiple-lenticular
Reversed-papillate
Multiple reversed-papillate
Multiple reversed-lenticular
74 (28)
1 (1)
21 (14)
1 (1)
16 (7)
-
Flat
6 (6)
38 (19)
12 (4)
11 (8)
2 (1)
3 (2)
13 ( 8 )
2 (2)
5 (4)
common. The mesophyll cells in petals with other kinds of epidermis are sometimes
similar in structure to this kind (e.g. in Chrysanthemum, which has a papillate
epidermis, and in Lampranthus, which has a flat epidermis) but are often rather
irregular, especially below the hypodermal layer. In nearly all cases, however, the
petal mesophyll is a more or less open aerenchymatous tissue with copious air-filled
intercellular spaces. The basic mechanism by which the mesophyll reflects light by
a combination of refraction and external and internal reflection was described by
Exner & Exner (1910), but very little is known of the optical properties of the
elements of the mesophyll. The efficiency of the mesophyll as a reflector varies in
different species, and the appearance of the mesophyll when it is exposed by
peeling off the epidermis also varies; the regular mesophyll of Chrysanthemum
coronarium, for example, has a shiny appearance (unidirectional reflection) whereas
Pelargonium zonale mesophyll shows diffuse reflection. These appearances may
however be artefacts.
In petals with carotenoid pigmentation, carotenoid-containing chromoplasts
commonly occur in the mesophyll, at lower concentrations than in the epidermis
but still in significant quantities that colour the tissue. Dissolved pigments
(anthocyanins, betalains and ultraviolet-absorbing flavonoids) are, however,
normally absent from the mesophyll, or occur only in insignificant quantities, in
most of the cases that we have examined, but there are some surprising exceptions
to this rule. Schubert (1925) was the first to observe and report petals in which the
visible anthocyanin pigmentation was actually confined to the mesophyll, and
absent from the epidermis (several members of the Boraginaceae). Most of the
cases that we have observed of this type have blue anthocyanin complexes in the
subepidermal layer of mesophyll cells; the epidermis appears to contain no
pigment, but in fact contains ultraviolet-absorbing flavonoids (as for example in
Echium, Myosotis and other blue-flowered members of the Boraginaceae, and in
Scilla tubergeniana and Chionodoxa cretica in the Liliaceae-Scilleae). The petals of the
Boraginaceae appear intensely blue and it is clear that a substantial proportion of
the incident light must pass through the blue pigment contained within the outer
mesophyll cells in these species. These mesophyll cells are morphologically
different from the corresponding mesophyll cells in species with unpigmented
mesophyll, in that pronounced projections are confined to their inner faces instead
FUNTIONAL ANATOMY OF PETALS
81
of occurring on all faces. It seems possible that in these cases the absence of
projections may be correlated with decreased surface reflection and hence
increased absorption of incident light by the pigment-containing outer mesophyll
cells. Thus, the surface projections of mesophyll cells, unlike the papillae of the
petal epidermis, may aid surface reflection.
The reflective mechanism in the petals of most yellow-flowered Ranunculus
species is different and is very distinctive. Here light is reflected by starch-grains
within the upper mesophyll cells, and light reflection does not require intercellular
air-spaces, although these may be present and may supplement reflection. The
reflective starch layer of Ranunculus petals was first described by Schimper (1885)
and Mobius (1885) and was independently rediscovered by Exner & Exner (1910).
Reflective starch layers of this kind are rare; we have observed a similar layer in
Anemone species, but we have found air-containing reflective mesophyll lacking
starch in Ranunculus peltatus and other white-flowered species in the genus, and also
in Caltha palustris. Most yellow-flowered Ranunculus species have an unusual flat
epidermis, but Ranunculus gramineus has a papillate epidermis above the reflective
starch layer, as do Anemone heldreichii and A . naorosa. Parkin (1928, 1931, 1935)
made an extensive study of the morphology and taxonomic distribution of the
starch-containing layer in the petals of Ranunculus and related genera, but rather
surprisingly did not appear to understand its function as a reflector, which is
independent of the unusual glossy petal surface of many Ranunculus species. Parkin
found starch layers in all of the 33 yellow-flowered Ranunculus species that he
investigated, but in only two out of nine white-flowered Ranunculus species. He also
found a strong starch layer in the closely related genus Oygraphis, and weak starch
layers in Adonis and Callianthemum, but did not investigate genera outside the tribe
Ranunculeae.
General discussion
Knowledge of petal structure and function is still far from complete. The range
of structures that occur in nature and their distribution among different taxonomic
and ecological groups are poorly known. The relationships between the
pigmentation, structure and surface micromorphology of petals and their functions
are still poorly understood. Much more work is needed, with implications for
several fields of biology.
Petal structure and function is of great importance in pollination biology, and
analyses of the relationships that may exist between the adaptive complexes of
petals and the.biology of the whole flower or inflorescence may be very productive.
For example, our preliminary SEM examination of the petal surfaces of typical
bee-, bird-, bat-, moth-, fly- and butterfly-pollinated flowers in the Polemoniaceae
suggests that there is a broad correlation between petal surfaces, anthocyanin
characteristics (Harborne & Smith, 1978) and pollinating agents (Grant & Grant,
1965).
The whole question of the relationships between papillate and reversedpapillate petals, which appear to represent different adaptive complexes, is of great
interest, as is the problem of the relative rarity of multiple-papillate petal
epidermises. The possibility that other adaptive complexes may exist, especially
among tropical plants (for example the translucent orchid perianths described by
82
Q. 0. N. KAY ET AL.
Exner & Exner, 1910) requires investigation. Scarcely anything is known, in
precise terms, of the structure and function of the petal mesophyll, and here again
it is possible that different adaptive complexes exist among petal mesophylls, and
that other reflective mechanisms exist in addition to the two basic kinds that are
already known.
Further work is also required on the nature and consequences of pigment
localization in petals. Until recently, the localization of compounds in intracellular
fluid compartments, such as vacuolar sap and the cytosol, were established by
histochemical and spectrophotometric analyses. But since 1977, it has become
possible to analyse these compartments more directly, by isolating intact vacuoles
and a fraction enriched in cytosol, or by quantitatively comparing the contents of
vacuoles and entire protoplasts (Wagner, 1979). The value of such a direct
approach is seen in Wagner’s recent study in which he reported, among other
topics, the vacuolar/extravacuolar distribution of anthocyanins in petal protoplasts
and showed that vacuoles isolated from Tulipu and Hippeastrum petals contained all
or essentially all of their anthocyanin pigment. Despite several difficulties discussed
by Wagner (1979) this method of analysis may be extremely valuable in
investigating pigment distribution in delicate petal tissues quantitatively, at the
intracellular level.
A better understanding of the relationships between petal structure,
pigmentation, function and appearance is of potential importance both in
evolutionary studies and for plant breeders concerned with the production of new
cultivars of ornamental plants. Desirable attributes of petal structure could be
identified and then searched for among existing cultivars and wild populations of
related taxa. Genotypically determined attributes of petal structure could then be
combined by the usual genetical techniques on a rational basis, in the same ways in
which petal pigment genotypes are combined. Related processes may occur in wild
populations as a result of natural selection. Plant breeders should be able to
produce new or extreme kinds of petal structure that are at a selective
disadvantage in wild populations but may be desirable in ornamental plants; it
might be possible to produce new petal structure forms by techniques which are
analogous to the production of new pigment varieties by the merging of different
biochemical pathways (Straw, 1956; Smith & Levin, 1963; Harborne, 1978).
Finally, the structure and surface micromorphology of petals provide engineers,
designers, architects and artists with patterns and structures that may be new and
may in some cases have important applications in optics, solar energy capture and
materials science.
REFERENCES
ARDITTI, J. & FISCH, M. H., 1977. Anthocyanins of the Orchidaceae: distribution, heredity, function,
synthesis and location. In J. Arditti (Ed.), Orchid biology: reviews andpnspcctivcs: 117-155. Ithaca: Cornell
University Press.
BAAGBE, J., 1977a. Microcharacters in the ligules of the Compositae. In V. H. Heywood, J. B. Harborne & B.
L. Turner (Eds), The biofogy andchnislry ofthe Comfisilac, I: I l S 1 3 9 . London & New York: Academic Press.
BAAGBE, J., 1977b. Taxonomical applications of ligule microcharacters in Compositae. I . Anthemideae,
Heliantheae and Tageteae. Botanisk Tidrskrii, 71: 193-223.
BAAGBE, J., 1978. Taxonomical applications of ligule microcharacten in Compositae. 2. Arctotidae, Asterac,
Calenduleae, Eremothamneae, Inuleae, Liatrae, Mutiseae and Senecioneae. Botanisk Tidrskrii, 72: 125- 147.
BARTHLOTT, W. & EHLER, N., 1977. Raster-Elektronen-Mikrowopie der Epidermis-Oberffachenvon
Spermatophyten. Tropuche und subtmpuchc gPanzenwzlt, 19: 1-105.
FUNCTIONAL ANATOMY O F PETALS
13
BLANK, F., 1947. The anthocyanin pigments of plants. Botanical Review, 13: 241-317.
BREHM, B. G. & KRELL, D., 1975. Flavonoid localization in epidermal papillae of flower petals; a specialized
adaptation for ultraviolet absorption. Science, New t'ork, 190: 1221-1223.
CALDWELL, M., 1971. Solar UV radiation and the growth and development of higher plants. In A. C. Giese
(Ed.), Photnphysiology, 6: 131-177. London & New York: Academic Press.
DAOUD, H.S., 1980. The roles of petalpigments and structure in producing ultraviolet colours andpatterns inyellow and white
Jowers. M. Sc. Dissertation, University of Wales.
EHLER, N., 1975. Beitrag zur Kenntnis der Mikromorphologie der Corollepidennen von Stapelieen und ihre
taxonomische Verwertbarkeit. Jahrbuch. Akadmie der Wissenschaften und dcr Literatur in Mainz, 15: 83-1 39.
EHLER, N., 1976. Struktur und Funktionen der OberRachen von Orchideenbliiten. In K. Senghas (Ed.),
Proceedings, 8th World Orchid Conference, Palmengarten, Frankfurt, 456-462. Frankfurt am Main : German Orchid
Society.
EXNER, F. & EXNER, S., 1910. Die physikalischen Grundlagen der Bliitenfarbungen. Sitzungsbnichte der
Akademie dcr Wissenschaften in Wien, Mathrmatirch-natunuus~c~ftluhe
Klarse, Abteilung I, 119: 191-245.
GRANT, V. & GRANT, K., 1965. Flower Pollination in the Phlox Famib. New York: Columbia University Press.
HABERLANDT, G., 1914. Physiological Plant Anatomy. London: Macmillan.
HALL, D. J., SKERRET, E. J. & THOMAS, W. D. E., 1978. Critical point drying for scanning electron
microscopy: a semi-automatic method of preparing biological specimens. Journal of Mkroscopy, 113: 277-290.
HARBORNE, J. B., 1967. Comparative biochemistry of thej7auonoiiis. London & New York: Academic Press.
HARBORNE, J. B., 1975. Biochemical systematics of flavonoids. In J. B. Harborne, T. J. Mabry & H. Mabry
(Eds), Thej9avonoids 105&1095. London: Chapman & Hall.
HARBORNE, J. B., 1977. Flavonoid profiles in the Compositae. In V. H . Heywood, J: B. Harbome & B. L.
Turner (Eds), The biology and chemistry of fhe Compositae, I: 359-384. London & New York: Academic Press.
HARBORNE, J. B., 1978. The rare flavonoid isoetin as a yellow flower pigment in Hlywoodiclla oligocephala and in
other Cichoriae. Phytochemirtry 17: 915-917.
HARBORNE, J. B.. & SMITH, D. M., 1978. Anthochlors and other flavonoids as honey guides in the
Compositae. Biochemical $ystematicsand Ecology, 6: 287-291.
HILDEBRAND, F., 1863. Anatomische Untersuchungen iiber die Farben der Bluthen. Jahrbuch fur
wusenschaftliche Botanik, 3: 59-75.
HILLER, G . H., 1884. Untersuchungen iiberdie Epidennisder Bliitenblatter.Jahrbuch fur wissenrchaftluheBotanik,
15: 411451.
KAY, Q. 0. N., 1979. Ultraviolet photography of the colours and patterns of flowers. Watsonia, 12: 339-340.
KEVAN, P. G., 1978. Floral coloration, its colorimetric analysis and significance in anthecology. In A. J.
Richards (Ed.), The Pollination of Flowers !y Insects, 51-78. London & New York: Academic Press.
KNOLL, F., 1938. u b e r den Samtglanz der Blutenblatter. Phobgraphie und Forschung, 2: 137-148.
KULLENBERG, B., 1961. Studies in Ophrys pollination. <oologiska bidrag fran Uppsala, 34: 1-340.
LOOMIS, W. D. & CROTEAU, R., 1973.Recent Advances in Phytochmistry, 6. London & New York: Academic
Press.
MABRY, T . J., MARKHAM, K. R. & THOMAS, M. B., 1970. hesystematic identlficatwnflJauonoids.New York:
Springer-Verlag.
MOBIUS, M., 1885. Ueber den Glanz der gelben Ranunculus-Bluten. Botanisches <entralblatt, 23: 115-1 19.
MULLER, L., 1893. Grundzuge einer vergleichenden Anatomie der Blumenblatter. .'Vova acta Academiae Caesareac
I.eopoldino Carolinae germanicae naturae curiosum, 59: 1 -356.
PAECH, K., 1955. Colour development in flowers. Annual Review of Plant Physiology, 6: 273-298.
PARKIN, J., 1928. The glossy petal of Ranunculw. Annals of Botany, 42: 739-755.
PARKIN, J., 1931. The structure of the starch layer in the glossy petal of Ranunculur. I. Annals ofBotany, 45:
201 205.
PARKIN, J., 1935. The structure of the starch layer in the glossy petal of Ranunculw. 11. Annals oJBotany, 49,
283-289.
ROBERTS, A. V. & HUMPHREYS, J., 1980. Colour in Roses. .~ationalRoseS~icly'sRose
Annual, 1980: 133-136.
ROLLER, K., 1956. u b e r Flavonoide in weissen Blumenblattern. <eitschriJifur Botanik, 44: 477-500.
SCHIMPER, A. E. W., 1885. Untersuchungen iiber die Chlorophyllkorper und die homologen Gebilde. Jahrbuch
fur wissenrchaftliche Botanik, 16.
SCHUBERT, K., 1925. Zur Kenntnis der Bliitenblatt-Epidermis. Botanischs Archiv, 12: 226-289.
SMITH, D. M. & LEVIN, D. A,, 1963. A chromatographic study of reticulate evolution in the Appalachian
Asplenium complex. Amnuan Journal of Botany, 50: 952-958.
SOLEREDER, H., 1908. $ystematic anatomy of the Dicopledons, 2. Oxford: Clarendon Press.
STEWART, R. N., NORRIS, K. H. & ASEN, S., 1975. Microspectrophotometric measurements o f p H and p H
effect on colour of petal epidermis cells. Phytochemistry, 14: 937-942.
STICKLAND, R. G . , 1974. The nature of the white colour of petals. Annals of Botany, 38: 1033-1037.
STIRTON, C. H., 1980. Petal sculpturing. In R. Polhill & P. Raven (Eds), Advances in lcgumesystmatics. London:
HMSO.
STRAW, R. M., 1956. Floral isolation in Penstemon. Ameruan Naturalisf, 90: 47-53.
WAGNER, G. J., 1979. Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and
anthocyanin in protoplasts. Plant Physiology, 64: 88-93.