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Botanical Journal of the Linnean Society ( 1992), 108: 35-4 7. With 6 figures
Differences in the location of subcotyledonary
buds among Epilobiurn angustifoliurn L.,
E. dodonaei Viii. and E. Jleischeri Hochst.
(Onagraceae) and effects on architecture and
population structure
JURG STOCKLIN
Botanisches lnstitut, Schiinbeinstr. 6, CH-4056 Basel, Switzerland
Received October 1989, revised and accepted for publication February 1990
J., 1992. DifFerences in the location of subcotyledonary buds among
Epilobium aragustifolium L., E. dodoraaei Viii. and E.fteischeri Hochst. (Onagraceae) and
effects on architecture and population structure. Morphological and architectural features in
the two closely related pioneer plant species Epilobium dodonaei and E. jleischeri are examined in
cultivation and in the field and compared with E. angustifolium. In E. angustifolium, the aerial shoot
STOCKLIN,
system is renewed every year from buds on horizontal roots and results in a horizontal spread and a
clonal growth form. In E. dodonaei, bud formation is restricted to the hypocotyl and in larger plants
to the transitional region between root and shoot. Consequently this species shows no vegetative
mobility and develops a shrob-like habit. The alpine E.jleischeri combines the habit of
E. angustifolium and E. dodonaei and may either develop successive generations of shoots from the
transitional region between root and shoot and/or exploit new areas by horizontal roots and the
formation of shoots from root buds. The simple difference in the location of renewal buds is
accentuated by cumulative growth. The study shows that E. dodonaei and E.jleischeri, which often are
considered as subspecies, are separated by fundamental differences in their architectural models.
The ecological and demographic implications of these differences are discussed.
ADDITIONAL KEY WORDS:-Epilobium - Onagraceae - subcotyledonary buds - clonal
growth.
CONTENTS
Introduction .
The plant species
Material and methods .
Results
Position and character of subcotyledonary buds
Population structure and architecture in the field
Discussion .
Acknowledgements
References
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INTRODUCTION
One of the characteristics of plants is their ability to form new embryonic
regions during their whole lifetime. Typically, these meristems are buds in the
axils of leaves. However, buds also occur frequently on the hypocotyl and on
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©
1992 The Linnean Society of London
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J. STOCKLIN
roots and this led Troll ( 1937) to consider this ability as part of the 'Bauplan' of
angiosperms. In contrast to the formation of axillary buds, which is governed by
phyllotaxis, the formation and number of subcotyledonary buds seem to follow
few morphological rules and is not precisely determined. From a comprehensive
study, Rauh ( 1937) concluded that subcotyledonary bud formation usually
starts on the hypocotyl and extends to roots. Several authors (Rauh, 1937;
Hagemann, 1983) showed that in closely related species, differences in the
formation of subcotyledonary buds may follow slightly different rules, resulting
in quite different plant architecture. Plants therefore, not only show considerable
plasticity in size and architecture due to modular growth by axillary bud
production (Harper & White, 1974; White, 1984), but also due to their
production of subcotyledonary buds. Shoot initiation, which comes not from a
basal region of former shoots but from buds on horizontal roots as in
E. angustifolium, results in a horizontal spread of the plant and in a clonal growth
form which explains to a large extent the colonizing success of this species
(Henderson et al., 1979). The question arises as to what extent subcotyledonary
bud formation is correlated with ecological differences between the closely
related E. dodonaei and E. jleischeri and how far it may explain their population
structure and differences in geographical distribution. The aim of this study is to
examine this question by recording morphological and architectural features in
E. dodonaei and E. jleischeri in cultivation and in the field and comparing these
measurements with the population structure of the investigated species in the
field.
THE PLANT SPECIES
Epilobium angustifolium L., E. dodonaei Viii. and E. fleischeri Hochst.
(Onagraceae, section Chamaenerion) are perennial herbs that colonize open
habitats. Their aerial shoot system is renewed every year from subterranean
buds. The general biology of the circumpolar E. angustifolium is well known
(Mosquin, 1966; Myerscough & Whitehead, 1966, 1967; Henderson et al., 1979).
Rauh ( 1937) showed that the yearly renewal of shoots in E. angustifolium occurs
from root buds and that in addition to a large seed output, long horizontal,
rhizome-like roots bearing buds lead to a growth form, which explains the ability
of this species to colonize recently-disturbed soil. Epilobium dodonaei and
E. fleischeri differ mainly in their altitudinal distribution. Epilobium dodonaei occurs
in Europe from France to W. Ukraine at altitudes usually below 1000 m, on
flood plains or gravel pits. Epilobiumjleischeri is restricted to the Alps at altitudes
between 1000 and 2200 m in the inundation zone of alpine rivers and is one of
the first pioneers on the perimeter of glaciers. Epilobiumfleischeri was considered as
a variety of E. dodonaei by Haussknecht ( 1884) and later gained the status of
subspecies (Schinz & Keller, 1923). Today, it is considered by most authors to be
a distinct species (Oberdorfer, 1983; Hess & Landolt, 1977). According to Raven
( 1976), E. dodonaei and E. jleischeri might be regarded together with E. colchicum
Alboff and E. stevenii Boiss. as subspecies of a polymorphic species.
Nat ural hybrids between E. dodonaei and E. fleischeri, which replace each other
altitudinally in the Alps, have occasionally been reported and Theurillat ( 1979),
in a biosystematic study, artificially obtained fertile hybrids and proposed to
reinstate E.jleischeri as a subspecies of E. dodonaei. Neither Haussknecht (1884)
SUBCOTYLEDONARY BUDS AND POPULATION STRUCTURE
37
nor other authors, in their considerations of the taxonomic status of E. dodonaei
and E. jleischeri, compared their mode of yearly root renewal, although the
question was raised very early by Irmisch (1857) and Rubner (1908).
MATERIAL AND METHODS
The growth forms of E. angustijolium and E. jleischeri were investigated at sites
in the Alps and E. dodonaei in the surroundings of Basel and the flood plains of
the Maggia in the Ticino. In addition, between 60 and 80 plants each of the
three species were grown from seeds in the glasshouse and replanted in the
experimental garden. For E. angustifolium, seeds were collected in the Black
Forest near Todtmoos, 30 km N.E. of Basel (elevation 950 m) and in the Alps in
the Vorderrheintal near Tschamut (1650 m). Seeds of E. dodonaei were collected
in the flood plains of the Maggia near Someo in the Ticino (380m) and from
ruderal sites in Pratteln and Huninque in the close surroundings of Basel
(280m). Lastly, seeds of E. jleischeri, were collected near Engelberg in the
Northern Alps (1100 m) and on the perimeters of the Rhone- and
Morteratschglacier in the Central Alps ( 1750 and 1900 m, respectively). To
study growth under different nutrient conditions, plants were cultivated in two
soil types, in a 1 : 1 mixture of sand and gravel and in garden soil enriched with
compost. Plants were examined at different ages and growth stages and height,
number and size of leaves, and inflorescence size were recorded. To study shoot
initiation, plants were excavated in the autumn and the position of buds and
characteristics of perennating organs were observed. In the field, growth
characteristics of individual plants, height, branching pattern, shoot number per
plant, number of fruits and weight of seeds were measured. Also seedlings were
excavated and compared with the plants in the experimental garden. Drawings
of perennating organs to show characteristics of shoot initiation were made from
plants grown in the garden at the end of the first growing season. Seedlings for
drawings were collected at field sites. In this paper the term 'architecture' is used
in the sense ofTomlinson (1987) as the momentary expression ofplant form and
is based on the concept of the architectural model, which refers to a genetically
determined growth plan.
RESULTS
Position and character of subcotyledonary buds
Plants of E. angustijolium grew only in garden soil; in a mixture of sand and
gravel they did not develop and died at the seedling stage. Epilobium dodonaei and
E. jleischeri developed differently in the two soil types: growth parameters for
these two species are given in Table 1.
The position of subcotyledonary buds in E. angustijolium, E. dodonaei and
E. jleischeri differ characteristically. Figures 1-3 show the root system and
transitionary region between the hypocotyl and the main root of plants grown in
garden soil at the end of the first growing season. Shoots of E. angustijolium are
always borne from root buds. The buds are formed endogenously on horizontal
roots, often but not exclusively where lateral roots branch off (Fig. l). Buds are
formed acropetally, i.e. the youngest are formed near the root tip. Seedlings only
J.
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TABLE
STOCKLIN
I. Growth parameters of E. dadanaei and E. jleischeri grown in two soil types
E. jl.eischeri
E. dodonaei
Sand/gravel
Garden soil
Sand/gravel
Garden soil
Size after 40 days:
Height (mm)
Number of leaves
Size of leaves (mm)
30-55
6
12 X 2
30-65
8
15 X 2
Up to 50
8
9 X 1.5
Up to 40
8
16 X 2
Size after 3 months:
Height (mm)
Number of leaves
Size of leaves (mm)
70-90
12-15
30 X 2.5
110-120
20-30
50x4
45-90
9-15
15 X 2
100-140
14-21
30x4
0
50-200
0
10-40
2
4-5
4-5
8-9
2
4-5
3-4
7-10
Flower and fruits
In autumn:
Basal diameter of primary axis (mm)
Number of buds
60 days old show buds protected by small scales on the main root. Whether the
plants set seeds in the first year or not, the primary axis dies away and root buds
grow out by the end of the vegetative period and develop underground. These
buds form colourless, fleshy sprouts 1-10 em long, which in the next year will
develop into aerial shoots. On plants grown from seeds in the garden, developing
buds could be found at more than 1.5 m from the primary axis by the end of the
first growing season.
By the end of the growing season buds in E. dodonaei develop exclusively on the
hypocotyl or the proximal part of the primary root. The buds are intensely red
coloured. Seedlings in the field mostly show two buds positioned at the upper
end of the thickened hypocotyl, the cotyledons being abscised long before bud
formation (Fig. 4). Larger plants from the garden carry up to 12 buds in the first
year, these being concentrated in a region at about the soil level either on the
proximal end of a tap root and the hypocotyl or at basal parts of branches of the
primary shoot (Fig. 2). Therefore, larger plants perennate by a tap root and the
basal remains of subsequent shoots, forming a multiheaded perennating organ of
considerable size in subsequent years. The perennating parts also serve as storage
Figure I. Root system with developing buds of Epilobium angustifolium: I. remaining part of primary
axis; 2. long horizontal roots; 3. fine root; 4. developing buds.
SUBCOTYLEDONARY BUDS AND POPULATION STRUCTURE
39
I em
H
Figure 2. Tap root of Epilobium dodonaei with buds on a region between root and shoot: I. remaining
part of primary axis; 2. basal remaining of side shoot; 3. tap root; 4. developing buds.
organs, large individuals in the field developing up to 100 1-m tall shoots every
year. Of more than 60 cultivated plants of E. dodonaei not a single one was
observed with buds on roots.
Epilobium fieischeri (Fig. 3) combines the habit of E. angustifolium and
E. dodonaei. The first developing buds in seedlings from the field (Fig. 5) are the
axillary buds of cotyledons; subsequently buds develop at the hypocotyl or in the
transitional region between root and shoot, and on roots. Buds develop
acropetally, therefore small plants in the first year have a tendency to form buds
primarily in the transitional zone between root and shoot. In the field, large
plants may be found which show a similar compact growth habit to that of
E. dodonaei, i.e. subsequent shoot initiation on a transitional region between root
and shoot and therefore forming compact clusters of shoots. But more often, due
to shift of bud formation to roots, individual plants consists of a more or less loose
system of shoots connected by roots. Moreover, in the field as in cultivated
plants, long horizontal roots with shoots developing from buds are a common
feature in E. fieischeri. The subterranean part of such shoots may thicken and
become a storage organ bearing buds and thus develop into a new multistemmed cluster in subsequent years. Root connections persist but are difficult to
excavate because they are long and break easily. It is not obvious if
environmental factors exist that promote a more compact or a more spreading
growth. In the garden all plants of E.fieischeri~with the exception of some
stunted ones~formed buds on roots. This capacity is part of the norm of
reaction of this species regardless of the biotope of the plant.
J. STOCKLIN
40
B
c
Figure 3. A. Root system of Epilobiumjleischeri with buds both on a region between root and shoot
and on roots. B. Detail of region between root and shoot. C. Detail of developing buds on the root. l.
Remaining part of primary axis; 2. horizontal root; 3. root; 4. buds on transitional region between
root and shoot; 5. developing root buds.
Population structure and architecture in the field
Performance of natural populations of the three species is governed by the
contrasting formation of renewal shoots. In addition, the growth form of the
three species is characterized by differences in apical dominance. In Fig. 6 the
characteristics of population structure are shown schematically and in Table 2
the architecture of E. dodonaei and E. jleischeri is compared.
SUBCOTYLEDONARY BUDS AND POPULATION STRUCTURE
41
Figure 4. Seedling of Epilobium dodonae1 at the end of first growing season. Note buds at the upper end
of the thickened hypocotyl: I. renewal bud; 2. hypocotyl; 3. primary root.
TABLE
2. Architectural features of E. dodonaei and E. jleischeri
E. dodonaei Viii.
E. jleischeri Hochst.
Basic module of aerial
shoot system
Prostrate to erect highly branched
Orthotropic usually unbranched
shoots up to 1.2 m tall, with elongated shoots up to 0.4 m tall, with short
inflorescences, flower buds lateral
inflorescences, flower buds lateral
Inflorescence size
30-40 fruits on main axis, up to 110
fruits on branched shoots
8-12 fruits on main axis, up to 80 fruits
on branched shoots
Yearly shoot renewal
From buds on the hypocotyl or in
larger plants from buds on the
transitional region between root and
shoot
From subcoty!edonary buds on the
transitional region between root and
shoot or on roots, especially on long
horizontal runners.
Perennating organs with
storing capacity
Tap root with the basal remains of
subsequent years' shoots
Tap root with the basal remains of
subsequent years' shoots and/or long
horizontal runners bearing buds
Adult plant form
Compact clumps of shoots with a
shrub-like habit
Compact or loose clumps of shoots,
even single shoots connected by roots
Clonal growth
No clonal spread, plants increase only
in size and shoot number with age
Clonal spread by iteration, new shoot
systems formed by bud formation on
long horizontal roots
Maximal cluster size
Up to 100 shoots with c. 4000 fruits
and 300 000 seeds
0.33-0.47 mg
Up to 50 shoots with c. 800 fruits and
60 000 seeds
0.11-0.21 mg
Weight of seeds
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J. STbCKLIN
Figure 5. Seedling of Epilobiumjleischeri at the end of the first growing season. Note renewal buds in
the axis of cotyledonary buds: I. cotyledon; 2. hypocotyl; 3. primary root.
As a consequence of its clonal growth form, populations of E. angustifolium
occur usually in dense stands and it is difficult to determine the size of clones.
Shoots are connected by horizontal roots and grow up to 1. 7 m in height and
mature up to 100 fruits each on an elongated inflorescence. Under natural
conditions, shoots are usually unbranched, but in rare cases basal side shoots
rna y grow out.
Populations of E. dodonaei are composed ofplants of different heights and shoot
numbers. The formation of buds on the hypocotyl and the transition zone
between the root and shoot results in dense clusters of shoots sitting on a tap root.
With increasing size, individual plants of E. dodonaei acquire a shrub-like habit.
Individual shoots show strong apical dominance and grow upright to more than
1 m. Branching normally occurs only in shoots longer than 70 em, basal side
shoots being the longest. Inflorescences are elongated and may develop more
than 30 fruits on the main stem alone. Small plants with less than four or five
shoots remain shorter than 20 em and normally do not flower. Nevertheless, they
make up 50-75% of all individuals in the observed populations. Most
reproducing individuals carry 5-50 fruits with 400-4000 seeds. A few very large
plants produce up to 4000 fruits with 300,000 seeds. These individuals contribute
the overwhelming part of the total seed output in a population. If there is open
soil, seedlings are commonly found on natural sites.
Populations of E. fleischeri are composed of either more compact plants with a
tap root or of more distributed shoots or clusters of shoots due to bud formation
on the root system. Often clusters of shoots of different size and shoot number or
single shoots are connected by long horizontal roots and therefore clones can
SUBCOTYLEDONARY BUDS AND POPULATION STRUCTURE
8
Figure 6. Schematic representation of population structure of A. Epilobium angustifolium, B. Epilobium
dodonaei and C. Epilobium j/eischeri.
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J.
STOCKLIN
hardly be discerned. In the field these connections are usually maintained but
occasionally they break especially in disturbed sites. In E. fleischeri as well as in
E. angustifolium damage to parts of the root system which become exposed
initiates regeneration shoots which quickly recolonize after a disturbance. This
capacity could not be observed in E.dodonaei which does not seem to develop new
buds when damaged. Shoots of E. jfeischeri vary from prostrate to erect forms
without a marked inhibition zone meaning that they are highly branched.
Branching from axillary buds may already occur in the first year when the
seedling becomes more than 7-10 em tall. Shoots normally reach a height of
20-40 em. Inflorescences are relatively short and carry up to 10 fruits on the
main stem and between 1-4 fruits on each branch. Single shoots taller than
10 em may produce flowers and fruits but only in rare cases does a cluster of
shoots produce more than 200 fruits with 15 000 seeds. Seedlings desiccate easily
in drought and are restricted to wet sites. However, because of deep reaching
roots, plants, once established, can persist even under drier conditions or until
shrubs and trees dominate in the succession. On the perimeter of the studied
glaciers this may last between 50 and 120 years.
DISCUSSION
In this study it has been shown that the location of subcotyledonary buds in
the three closely related Epilobium species varies in such a way that it results in
different plant architectures and population structures. In E. angustijolium the
shoots are renewed every year exclusively from root buds, which are formed
mainly on long horizontal roots. This results in a mainly horizontal growth and
clonal spread. Individuals of E. angustijolium can explore and exploit a habitat
once occupied and there is maximal use of sexually produced genotypes after
rigorous selection at the seedling stage. Henderson et al. ( 1979) estimated that,
once established, plants of E. angustijolium allocate up to 60% of their
photosynthate to roots and Van Andel (1975) showed that young populations
may not only expand 1-2m each year, but can persist for many years because of
a mineral cycle brought about by the population itself. Although no buds are
initiated from the hypocotyl in E. angustijolium, initiation of shoots in a 2-yearold plant are frequently close to the dead primary axis as a consequence of early
beginning of bud formation in an acropetal order. In subsequent years, shoots in
a dense population become distributed more or less regularly and the results of
growth experiments in different soils make it quite plausible that regulation of
bud development is determined by the availability of resources (personal
observation). In other species it has been demonstrated that the number of
regenerative buds depends on the lengths of roots (Bonnett & Torrey, 1975) and,
for instance, the diameters of roots in apple trees (Way, 1954).
Plants of E. dodonaei have no vegetative mobility and develop a shrub-like
habit. Bud formation is restricted initially to the hypocotyl, which serves
together with the tap root as a storage organ and within subsequent years
growth results in an increasing number of shoots of increasing height. The lack of
vegetative propagation permits a maximal production of seeds of considerable
weight (about ten times the weight of seeds of E. angustijolium). In E. dodonaei too
a large individual may contribute disproportionately to the next generation
because of the enormous increase of seed output with size. Smaller plants in a
SUBCOTYLEDONARY BUDS AND POPULATION STRUCTURE
45
population may increase genetic variability mainly by male function. Although
bud formation in E. dodonaei is restricted to a region between the root and shoot,
with increasing size this region comes to include basal parts of the shoot system.
This flexibility permits plants to persist even when rooted in mobile ground and
subject to limited burial. But since E. dodonaei lacks buds on its roots (and hence
regeneration from roots) this may explain why the plant does not occur on
heavily disturbed sites. Hess & Landolt ( 1977) reported that E. dodonaei does not
occur on regularly inundated parts of flood plains.
It is precisely such heavily disturbed areas which are preferentially colonized
by E. jleischeri, a plant occurring in the Alps, and usually at elevations higher
than 1000 m. This species can develop, year after year, successive generations of
shoots at one spot (as does E. dodonaei) and it has the capacity to exploit new
areas of soil by horizontal roots and the formation of root buds (as
E. angustifolium). Therefore, in contrast to E. dodonaei, populations are built up
clonally and as a consequence are very persistent. This clonal habit of E. jleischeri
appears to be an adaptation to the periodic disturbances which are frequent on
alpine river banks and the perimeters of glaciers where indeed E. jleischeri mainly
occurs. In addition, due to the harsh alpine environment the amount of seed
production varies from year to year depending on climatic conditions during the
period of seed maturation.
The ability to produce root buds must be considered in any discussion of the
taxonomical status of E. dodonaei and E.jleischeri. Kormanik & Brown (1967)
concluded that for trees the ability to produce root suckers varies widely between
species and is determined genetically. The formation of root buds is part of the
normal pattern of growth for E. jleischeri. Buds on roots were never found in
E. dodonaei, either in cultivation or in the field. This is in contradiction to
Oberdorfer ( 1983) who mentions the formation of stolons (Ausliiufer) in
E. dodonaei. In the older literature confusion between the two species is frequent,
because of the striking overall similarity between aerial parts which normally are
collected as herbarium specimens and considered alone in taxonomy. However,
the position of meristems or buds is crucial for the architecture of a plant (Halle
& Oldeman, 1970) and furthermore, its ecological properties may even depend
on it, as shown by Raunkiaer's (1937) system of classifying plants based on
meristem position. If the architectural models (Table 2) are taken into account,
it becomes clear that there is not only an overlap in many morphological traits
(Theurillat, 1979; Slavik, 1974), but that fundamental differences also separate
the two species. However, large differences in architectural characteristics can
result from small changes of the rules which govern plant growth (Tomlinson,
1982). White ( 1984) writes that in plants number and spatial disposition of
metamers are under relatively simple genetical control. This might be true also
for the formation of root buds. This simple morphological feature is accentuated
by cumulative growth and the perennial life cycle. The clonal growth habit of
E. jleischeri is expected to have further consequences on characteristic properties,
namely on sexual reproduction and diversity. In fact not only seed weight, but
also number of fruits per shoot and maximum fruits per plant are considerably
lower in E. jleischeri than in E. dodonaei. Slavik ( 1974) found a significantly higher
intraspecific variability in E. dodonaei than in E. jleischeri. It is likely that the
decreasing growing season with altitude contributes to the reduction in size and
numbers of seeds, but the same phenomenon also effects costs of clonal growth.
46
]. STOCKLIN
Altogether, the consideration of architectural characteristics emphasizes the
distinctness of the two taxa and justifies the separation of E. dodonaei and
E. Jleischeri as two distinct species.
The analysis of architecture is increasingly seen as important in the
understanding of ecological, successional and demographic processes in plants
(White, 1979; Bell & Tomlinson, 1980). In addition to merely looking at
morphology, a description of architecture and the underlying architectural
model reveals the developmental history of plant form. The research of Halle &
Oldeman ( 1970) greatly influenced this dynamic approach for trees and its
application to herbs now looks promising Ueannoda-Robinson, 1977). Since the
perennial habit in herbs is frequently linked to the occurrence of
subcotyledonary buds, this feature has to be considered in the architectural
description of herbs, as is shown in the present study. By simple differences in the
location of buds, which annually renew the aerial shoot system, two contrasting
forms are realized: clusters of shoots from one point, and horizontal (clonal)
growth of more or less distant single shoots. Because each bud, independent ofits
location on perennial parts of the plant, repeats the same process of reiteration as
the primary axis, both forms can be regarded as variants of Tomlinson's model
described by Halle & Oldeman ( 1970). The two forms illustrate the easy shift
from individual growth to clonal spread in modular constructed plants and in
fact represent two contrasting strategies of different ecological meaning and
fundamental demographic properties. Similar differences may be found in
rhizomatous herbs by different length or number of internodes (Schmid &
Bazzaz, 1990). It would be of special interest to study, what environmental
conditions favour a more compact or a more spreading population in E. jleischeri,
a species which shows a combination of both forms.
ACKNOWLEDGEMENTS
This study has been supported by the Swiss National Science Foundation
grant no. 3.631-0.87. I thank Esther Schreier for drawing the figures and
Andreas Erhardt, Donald Kaplan, Bernhard Schmid and Heinrich Zoller for
helpful comments on the manuscript.
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