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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 35 36 37 37 37 40 44 46 46 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 0024-4074f92f010035 + 13 $03.00/0 35 © 1992 The Linnean Society of London 36 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. 38 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 42 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. 43 44 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. 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