Adaptive architecture in rhizomatous plants

A. D. BELL

School of Plant Biology, L'niverszty College ofNorth Wales, Bangor, Wuler, li. K.

AND

P. B. TOMLINSON

Huruard Uniuerrity, Haruard Forest, Petersham, Massachusetts, U.S.A.

Thc. ,ir-c.tiitectuiw 01 Icw I himmatous plants has been studied in an\ morphologtral detail: a g1.e.it iniinv of those which have been studied show highly organired and repetitive hr.anc-hing pattern\. Thes;, 1)ranchiiig pattern\ ai-e largelv confined to thrre basic types: those based on a f 60' branc-hing angle, those hsed on a A 45' branching angle, and those with a predominately linrar componrnt. These vaiiou\ configui-ations must ronfer certain advantages in terms of substrate exploration and exploitation. The consistent architecture of many rhizomatous plants permits predictive graphi(- tiniulation of the branching patterns, and also permits estimates to he made ofproductlvltv in tcrni\ ol rriei-isteinistioot accumulation. As a background to this structural consideration of rhi&iatous plants, an rxtriicive bihliograptiv is presented in an appendix, covering all aspects ot rhizomatous and \toloriifei 011s gi owth.

KEY U'ORDS~-i-hi~o~ne-stolon-archirrcture-pattern-branching-geometrv-ce~~ellat~~~~~

CONTENTS Intl~oductlon ...... I1b Rhizornr definition ...... 126 Adaptive and telectiir tinits ... li7

Drtrrrninistic- versus opporturiistic~. patterns 120 Essenti,il nsprc-ts of rhizoinr organization ...... ,129 Occagonal gi-id, ...... I30 .Medeoln Iqiniann L. ITrilliareaeI ...... I YO Geoirirti-ical proprrtie, of the Medeola system ...... 133 Rhizoinr geometn ol~Ouali~...... 133 Hcxagonal grid\ ...... 131 Alpinin .rpe(tuin K. Schiiin. IZingiberaceae) ...... I34 Other- examples . . , . . , ...... I56 Lineal- sy\tcwir , , ...... 137 Zingibei-ale\ ...... 1 3 7 Cnrrv oreiinrin L...... I40 Seagrass rliiromes ...... 140 Shoot dimorphi\in ...... 119 Factoi-s infltientiiigpartt~rii ...... It3

Conipiitri- siniulation . . , , ...... 116

0024-4074/80/020125 + 36/$02.00/0 @ I980 The Linne,iii EocietT of London 126 A. D. BELL AND P. B. TOMLINSON

Conclusions ...... 146 Acknowledgements ...... 147 Refkrences ...... 147 Bibliographical appendix ...... 157

I NTRO DUCT1 ON

Demographic studies of plants are often made difficult because the plants may spread by both sexual and vegetative means: that is by open growth in contrast to the closed growth of higher animals where individuals have a fixed number of parts. Most plants, especially herbaceous perennials, can duplicate their apical meristems by branching. Subsequent dissociation of meristems following vegetative fragmentation may then make it difficult to identify the ‘individual’ for demographic study. Identification of the ‘individual’ may well depend on the circumstances of the investigation and the nature of the inquiry (Takhtajan, 1959; Flower-Ellis, 197 1 ; Egorova, 1972, 1973). The units of such fragmented plants are not fixed; they travel as they grow at the distal end and rot at the proximal end. They are also potentially immortal. These circumstances have been recognized for some considerable time (Royer, 18 70) and ‘creeping clumps’ must be a feature of a great many vegetational types (Lieth, 1960). However, the structural details of such clumps are commonly ignored and the plant is usually recorded simply as ‘rhizomatous’.

Rhizome definition We use the term ‘rhizome’ in a very general way to indicate vegetative extension over or within the substrate by means of axis elongation, and include organs which may be distinguished more precisely as stolons, offsets, or suckers and which may intergrade with tubers and corms. Where precise definitions are attempted (e.g., Warming, 1918; Holm, 1929; Burkill, 1960; Stevens, 1966), they tend to be insufficiently inclusive for our use. Rhizome, for example, in most connotations implies or is restricted to underground organs, thereby excluding many epiphytes which, by morphological standards, are frequently rhizomatous. Other definitions emphasize the perennating axis in terms of food storage (i.e., it is considered to be a fleshy organ) in contrast to more slender ‘stolons’. Although it is often useful to make a morphological distinction between rhizome (a thickened axis), stolon (an extended axis) and corm (a squat upright axis) there is no precise circumscription in terms of clone spread. Likewise rhizomes are not necessarily horizontal, since they may be descending as in Cordyline (Tomlinson 8~ Fisher, 1971) and Costus spectubilk K. Schum. (Holttum, 1955; N. Hallk, personal communication), ascending, as in many epiphytes (e.g., Araceae, Cyclanthaceae), or indeed both as in Polygonum bistortu L. (Chabot-Jacquety, 1967). Consequently, rhizome is a useful general term, readily qualified as fleshy, stoloniferous, aerial, descending, scale-bearing, leafy etc. Semantic obstacles arise only when the term is too rigidly defined. We exclude root-suckers from this article, justifiably on a morphological basis, but artificially in ecological terms, since they frequently carry out the function of vegetative mobility we discuss. Although morphological accounts of root buds are to be found in the literature (see Peterson, 1975, and Appendix, Section A), RHIZOMATOUS PLANTS 127 we have not found evidence for the precision in their distribution which exists in many rhizome ystems.

Adaptive and selective units Harper & White (1974) and Harper (1977) distinguished between ramets and genets. A genet is the product of growth of a seed without genetic recombination; a ramet is a separated vegetative part of this. A clone is thus a genet (in angiosperms, but not necessarily in cellular plants with a single apical cell, Klekowski 19761, and is usually composed of an ever-increasing number of ramets. Since natural selection is concerned with the preservation and modifica- tion of genotypes, it is the genet which is of value in the survival of the species but the ramet which frequently provides opportunity for extensive multipli- cation of a given genotype and enlargement of a population. This allows maximum exposure of the genet and maximum opportunity for exploitation and exploration of a diversity of habitats by vegetative spread. The population biologist sees asexual reproduction and vegetative propagation as the maximum use made of a sexually-produced genotype after rigorous selective screening (Williams, 1975). It seems realistic to assume that there are optimal ways in which asexual exploration inav be carried out, or optimal strategies of vegetative mobility. For ecological and population purposes the ultimate adaptiue unit of plant growth should be the shoot apical meristem itself, since this is often sufficient to generate all organs, provided that adventitious roots are readily developed by the stenis. However, the ultimate selective unit must be the sexually-produced seed- borne rneristern since this is, via the process of mutation and sexual recombina- tion, the source of genetic diversity upon which natural selection acts. Leaving aside the evolutionary need for genetic diversity, if the relative origins of adaptive and selective units are considered, it is clear that the vegetative process is likely to be much more efficient than the sexual process in dis- seminating and establishing meristems. A typical example of this is Mercurialis perennis L. (Mukerji, 1936). Cirsium arvense (L.) Scop. (Hayden, 1934) can also be cited as an example; although it produces prolific numbers of seeds, it is equally prolific in the number of root buds which then develop rhizomatously. A similar situation for Solidago species is described and discussed by Werner (1976). The chief function of adaptive devices of seed-borne meristems is dispersal, a process which removes a seed (or comparable propagule such as the seedling of mangroves) from the competitive sphere of its parent, temporally as well as spatially. Dispersal devices may be either lacking, or otherwise highly specialized so that long-range dispersal by wind, water or animals (especially birds) is possible (van der Pijl, 1969). However, very little of the actual mechanics of seed dispersal is concerned with placement of the propagule in an appropriate site, though incidental or supplementary devices may assist in the anchorage of the seed. Such devices include: the adherent seeds or fruits of many epiphytes or parasites (e.g., strangling figs, mistletoes); the adherent seed hairs of epiphytic Tillandsia species once they are wetted, although these hairs are primarily flotation devices; the grapnel-like organs of the fruit of the seagrass Amphibolis; the burying of dispersed seeds by ants (Handel, 1976, 1978) and rodents, or by hygroscopic movements (Erodium). Fruits are sometimes buried bv a negatively 12s A. D. BELL AND P. B. TOMLINSON geotropic or phototropic response, as in Arachis hypogaeu L. and Cymbalaria muralis Gaertn, Mey & Scherb. There is limited control of dispersal distance in plants with explosive fruits where the seeds may have a fixed trajectory (Beer & Swaine, 197 7 ; Swaine & Beer, 1977). Nevertheless site selection by seeds or fruits is essentially a chance process and the reproductive strategy of a plant can be seen as an attempt at a statistical guarantee for a process with enormous odds against success. In most cases, for a stable population to be maintained in a stable environment, only one offspring seed is required to grow to reproductive maturity from each progenitor. Thus the odds against survival of a seed need only be the reciprocal of the total reproductive capacity (in seed meristems) of a plant in order to guarantee this constancy, other things being equal. This chance can be expressed in very simple terms for the monocarpic palm (Coryphu) as 1:250,000, this being the calculated number of seeds produced by the palm after flowering (Tomlinson 8c Soderholm, 1975). Here the meristem unit is particularly appropriate since the palm remains vegetatively unbranched throughout its life (about 45 years), the single seed-borne meristem generating the total biomass of the palm. In this palm the wastage in terms of biomass (dry weight) can be demonstrated. A single seed has a dry weight of 2.3 g and yet between 500 and 700 kg of biomass goes into seed production, this representing an estimated 15% of the total biomass generated by the seed-meristem (Tomlinson 8c Soderholm, 1975). This disparity between bioenergetic effort and result is typical for plants. In contrast, site location via vegetative spread, where new ramets are placed at a greater or lesser distance from the parent axis by some method of branch extension in the substrate, is much more economical. Furthermore, the depth of ‘planting’ can be regulated (Massart, 1903 a, b). For example, in Oxalis cernua Thunb. ‘planting’ of bulbs is determined by limitation of bulb development to certain soil levels. This species (in which propagation is entirely by vegetative means, Galil, 1968) is unusual because both horizontal and vertical displacement occurs, the horizontal displacement resulting from the activity of a horizontal contractile root. In vegetative spread few meristems are involved, as the subsequent description indicates. It is difficult to determine how much the process ‘costs’, since branching is normally an integral part of ramet development. Undoubtedly the process is most efficient because directions and distances can be predetermined while large food reserves and a water supply are often maintained in the mature parental axis (Yin, Shen & Shen, 1958; Giddens, Perkins &Walker, 1962; de Byle, 1964; Qureshi & Spanner, 1971; Clifford, Marshall & Sagar, 1973; Nyahoza, Marshall & Sagar, 1973, 1974). There is the further possibility of feedback mechanisms which may be important in generalized flowering responses. There are disadvantages: new genotypes are not being selected, except in the case of lower plants in which there may be somatic mutation within single apical cells (Klekowski, 1976; Klekowski & Berger, 1976); and distant favourable habitats are not exploited. Only in stoloniferous plants may extension of up to several metres (e.g., Aralia nudicaulis L., North America) be possible between one unit and the next. Nevertheless, the clone itself may cover a considerable area, given time, and at least in its early stages of development have a definite shape (Zaugolnova, 1974; see also Appendix Section B). Excepting specific environmental constraints, any precise clone shape is the direct result of precise rhizome branching patterns. RHIZOMATOUS PLANTS I29 There is evidence that clones can reach considerable sizes, hundreds of metres in diameter in some cases (Ovington, 1953; see also Appendix Section C). Such clones must be of considerable age, which may be estimated bv dividing the radius of the clone by the average annual radial growth (Oinonen, 1967 a, b, c, 1968, 1969, 1971; see also Appendix Section D), or more accurately by deciphering anatomical or morphological features (Flamm, 1922; Molisch, 1938; Kershaw, 1960; Rabotnov, 1960). Actual long term studies of individual plants in the field are rare (Tamm, 1948; Epling 8c Lewis, 1952; Tamm, 1956; Canfieldl957; Tamm, 1972 a, b). Some age estimates for single clones are in excess of 1000 years. (Penzes, 1958, 1963; see also Appendix Section D.)

DETERMINISTIC VERSUS OPPORTUNISTIC PATTERNS We wish to emphasize the part played by the morphology of these plants, as this has a direct bearing on the size and age of clones, their productivity, and particularly on the overall and internal shape of the clone. Readers familiar with the concept of tree architecture, developed bv Hall6 & Oldeman (1970) and further extended in Hall6, Oldeman & Tomlinson (19781, may recognize the same principle of a genetically determined growth plan in our approach to the analysis of rhizome morphology. This is appropriate because the concept of architecture is applicable to all systems with organized form. Herbaceous plants, including rhizomatous, clone-forming plants, have been shown to conform to the basic principles of tree architecture developed bv Hall6 8c Oldeman (Jeannoda-Robinson, 1977). A more important concept, that of reiteration, established and developed by Oldeman (1974) (see Halli., Oldeman 8c Tomlinson, 1978) is essential. This recognizes the possibility of the repeated development of a plant's architecture as an environmental response, usually in the form of the release of latent meristems, not active in the normal architecture of the plant. This process is shown to be ecologically important in certain types of rhizome organization. Traumatic reiteration (Edelin, 1977) is a familiar response of many plants to partial destruction (e.g., Ueda, 1960; see also Appendix Section E). Adaptive reiteration (Edelin, 19771, i.e., the ability to repeat the basic architectural model of the plant in response to supra-optimal conditions, is a more difficult phenomenon to demonstrate, but it is important in the productivity of many rhizomatous plants (Noble, Bell 8c Harper, 1979; see also Appendix Section F). Branching of a shoot system can thus be thought of in terms of. seguential branching which determines the architecture and reiterative b_ranching which repeats the architectural model as discussed bv Oldeman (1974; see also Tomlinson, 1978).

ESSEYrIAL ASPECTS OF RHIZOME ORGANIZATION Geometric patterns of rhizome extension in plants may be recognized most easily if they are linear systems with branches which diverge at more or less precise angles in a single plane, with uniform increments of growth between the branch insertions. Three criteria are important. The position of a meristem or bud is often crucial to the subsequent direction of growth of that particular branch module (Gillet 8c Tinchant, 1964; see also Appendix Section GI. The part 130 A. D. BELL AND P. B. TOMLINSON that the development of the meristem plays in the overall pattern of the rhizomatous system depends on the timing of its commencement of activity, a feature which may be governed by apical control (e.g., McIntyre, 1964, 1965, 1969, 197 l), or more importantly by some mechanism of innate dormancy (e.g., Johnson 8c Buchholtz, 1957); a meristem with long dormancy is likely to develop when the active distal ends of its clone have migrated some distance away. The third criterion of rhizome organization concerns meristem potential. This is one of the essential features of Hall6 & Oldeman’s (1970) approach-different vegetative meristems, as a consequence of their different positions and time of growth, may develop into different types of structural units (Bowes, 1961 ; Cutter, 1967; Haslam, 1969; Fisher, 1972).This feature is more evident in trees but Fig. 8 illustrates it in seagrasses. Nevertheless in any plant, when a dormant meristem begins to develop, it will provide a structure reduplicating the whole or part of the original structure of that plant, and the pattern of the rhizome system will either be repeated or repaired. Superimposed on the intrinsic pattern of the plant’s architecture is a regulatory response to the immediate environment. In rhizomatous plants this is largely a response to depth adjustment and may involve sensitivity to factors such as light, water table, water pressure, oxygen or sand accretion (Clapham, 1945; see also Appendix Section HI. Meristem position is the basis of Raunkiaer’s (1937) system of classifying plant ‘form’ (see also du Rietz, 1931; Numata & Asano, 1959). The rhizomatous plant develops according to a basic architectural pattern and we can recognize three simple parameters in a rhizome system, a linear component, a component of divergence (from linearity) and a spacing component by means of which meristems or appendages are separated. These parameters provide the basis for numerical analysis. Analysis of rhizome architecture is fairly simple since secondary growth is either absent (as from pteridophytes and most monocotyledons) or so limited that the scars of older organs remain unobscured (as in many dicotyledonous herbs). It is then usually possible to chart the previous history of a persistent rhizome system by careful examination of appendage scars. However, there are few accounts that are sufficiently detailed and comprehensive to result in identification of basic patterns in the branching systems (McClure, 1966; see also Appendix Section I). Other morphological accounts of rhizomatous plants are not concerned with precise details of pattern but describe rhizome morphology to some degree, Caldwell(1957),and see also Appendix Section J. In other studies of rhizomatous plants, the morphological aspect is ancillary to the main theme of an investiga- tion (see Appendix Section K). Thus the recognition of basic pattern represents a significant advance in the understanding of the relationship between the rhizomatous plant and its environment which has hitherto passed largely unnoticed.

OCTAGONAL GRIDS Medeola virginzana L. (Trilliaceae) This species was analysed morphologically and in terms of its population dynamics by Bell (1974). Medeola virgzniana L. (Indian cucumber) is a summer- RHIZOMATOUS PLANTS 131 flowering herb, widespread in mixed deciduous forests in eastern North America, which overwinters entirely by means of its fleshy edible stem-tuber. The rhizome system (Fig. 1) is syrnpodial, each unit ending in an erect leafy shoot which may bear flowers. Each’annual increment is extended by a slender stolon ofwhich the tuber is the swollen continuation. Each increment dies and shrivels at the end of its summer leafing, tubers of the next generation providing the overwintering ,f ?!% unit. Consequently all rneristems are dissociated two years after thev are L.’+cdyb initiated, which allows ready population analysis in terms of meristems as ramet \ units. Spacing is provided by the annual extension of between 5 and 15 cms, determined largely bv the vigour of the shoot. In natural populations two daughter meristerns grow out each year causing spread of the population in preferred directions. Additional reserve meristems, not normallv extended, are formed, as discussed later. Measurements of a population in Central Massachusetts (Bell, 1974) showed that the linear component was the result of development of a distal bud growing in the same direction as the parent rhizome, the direction not being determined by phyllotaxis. Consequently a leafv shoot is erected annually at a linear distance determined by this component. Divergence is provided by the development of a second bud, proximal to the whole unit, i.e. at the proximal end of the stolon. Its morphological origin is somewhat obscure since it is not associated with a subtending scale leaf-again phvllotactic rules are not significant in branch orientation (cf Zohary, 1938). Initiated at the end of one summer, this meristem develops a new rhizome unit at an angle close to 45O to the direction of growth of the parental axis, establishing a new linear component. Each year a proximal bud is formed on the same side of the axis and its position ensures that a new shoot remains pivoted on the original site, but displaced by 45O, so making one complete revolution every eight vears, presuming that the rhizome system persists. Further symmetry is brought to the system because the proximal bud thrown off by each new linear component alternates from left to right in successive years. Consequently two vears and two increments elapse between each divergent component thrown off in the same direction bvI, anv one linear component. The essential features of this system, as seen from above, are presented in Fig. 1 on the assumption that all meristems develop and succeed according to this idealized pattern. The overall geometry of this method of spread consists of a series of potential octagons (consequent in the 45O angle of divergence, with the sides equal to twice the spacing component). Each site of meristem production, corresponding in summer to an erect leafv shoot, can persist by virtue of the proximal bud but the whole population spreads outwards progressively by means of distal buds. The pattern is clearly idealize’d, but equally represents the inherent growth potential of this system for vegetative mobility, that is, the architecture of‘ the system. It is capable of further analysis, as presented later. The geometrv of the system is not evident in nature because of the limited success of new meristems and the annual disconnection of successive rhizome generations. A degree of plasticity is admitted to the system since dormant meristems occur in the axils of additional scale leaves and these may grow out, when plants are damaged, or, as shown by Bell (1974), when tubers are grown in the supra- optimal conditions of a greenhouse. These ‘traumatic’ and ‘adaptive’ environmental modifications correspond to ‘reiteration’ in Oldeman’s ( 1974) sense of the word, this phenotypical modification of the inherent architecture m e CI 5 -1 -1 wm di RHIZOMATOUS PLANTS 173 resulting in the development of additional meristems not normal to the architecture 01‘ the svstern. These meristems repeat fully the architecture of the svstcni. Medeoln is particularlv instructive because it demonstrates all the features of vegetative mobility which we wish to emphasize. Alternative strategies which enlphasize different parameters are considered later.

Geometrical properties of the Medeola system Thc octagonal swteni implicit in Medeola can be viewed in terms of its abilitv to tesselate or ‘tile the plane’, in other words be treated as regular polvgons which may 01-rnay not be fitted together without intervening free space. Onlv three rcgular- polvgons, triangles, squares and hexagons have this proper-tv, determined tn the fact that their internal angle (60°, 90°, 120°) is an integral divisor- of 360’. Octagons (internal angle 135O) cannot be laid contiguouslv as tiles, but most over-lap. Transformed into rhizomatous terms, the branching angle of Medeola establishes a pattern which, if followed precisely, will ultimatelv explore a given area completely, without superposition of ‘meristerns. Ani nic+steni which reaches a favourable habitat by this means will persist bv virtue of the proximal tneristerns, which rotate around a fixed point, making (‘)nefull circle in eight generations. We can say that Medeola has a rhizome strategv suitable for its habitat as a woodland herb, since it persists largely by vegetative spread. However, ‘expenditure’ is minimal, since in each ramet generation onlv two riieristetiis are needed to establish the pattern. There is built into the system a degree of plasticitv, occasioned by the ‘reserve’ meristems which do not play an iniinediatc role ii; the pattern we have described, but are capable of initiating additional cycles of growth.

Rhizome geometry of Oxalis A second cxatnple of a rhizome pattern based on octagons (i.e.,a divergence angle of +_ 45Oi is provided bv the aggressive weed Oxalis corniculafa L. (Ox- alidaceae) illustrated diagrarnmaticallv in Fig. 2. In the post-seedling stage this has leafy rosettes with a 5/8 phyllotaxis, and axillary stolons tend to grow out in directions determined bv the arrangement of subtending leaves in eight orthostichies (Fig. 2A). FJrther leafy rosettes are established at points where a persistent tap root is sent down, these second-order rosettes functioning as generating centres radiating further stolons. In Fig. 2B only six of the eight possible directions of growth are being explored, indicating competitive interaction according to rules which have still to be elucidated. Reproductive

Figure 1. \fddn wrgzniann iTrilliaceae), plan view of rhizome svitein shown diagramaticaIl\. Each ‘individual’ is 1-eprrsentedbv a rhizome segment which in winter consists of a tuberous distal poi-tion .lid a proxiiiial stoloniferous portion with a basal bud. In sprlng this produces an el-ect leafv choot

A

0-0Stolon @ and @ Stolon or flower @ Stolon or dormant meristem

Figure 2. Oxalis corniculata (Oxalidaceae),plan view of seedling rosettes and the type and orientation of the lateral axes they subtend (from measured examples). A. Recorded orientation of first 6 foliage leaves, in which two possible arrangements and their mirror images are shown. The numbers indicate the potential behaviour of the bud in the axil of each leaf. B. Plan view of an actual stolon system in which six of the eight possible lines of growth have developed from the original seedling axis. The stolons themselves have branched further. efficiency is further promoted in this species because sticky seeds are dispersed from explosive capsules to distances of up to 3 m.

HEXAGONAL GRIDS Akinia speciosa K. Schum (Zingiberaceae) The most economical means of tesselation utilizes a regular hexagonal grid (Kepler, 161 1; Losch, 1954; Gardner, 19751, a geometrical pattern which can be found in the rhizome system of a number ofunrelated plants (Bell, 1979).Figure 3 illustrates this for Alpinia speciosa (shell ginger), a commonly cultivated member of the Zingiberaceae which is representative of many members of this family. The rhizome system consists of a series of scale-leaf bearing sympodial units, each unit growing horizontally via its apical meristem for a standard distance before turning to become erect as a foliage-bearing shoot, which terminates in an inflorescence. Adventitious roots are restricted to the base of the lea5 shoot. Rhizome extension RHIZOMATOUS PLANTS 7

/

Figure 3. Alpznfn ~~CLZOUI(Zirigiheraceae). Plan view of the ac-tual Ihimme svstem of thr-re sepal-ate plants. Earl1 unit or rhizome wgmmr is approximately 11 rm long. continues by the development of two new horizontal units arising from meristems in the axils of a pair of scale leaves at the base of the aerial shoot. These are always on opposite sides of the stem and it is this repeated Y-shaped branching which forms the hexagonal pattern. The rhizome segments can be regarded as spacers placing the aerial shoot and root complexes at the points of the hexagonal grid (Fig. 3). Observation shows that the aerial shoot of A&znza dies after three wars (or three syinpodial unit generations) whereas the rhizome segments persist for up to ten years before rotting. This allows one to construct a population grid developed by a single ramet (Bell, 1979) in which it is assumed that all branch meristerns are successful, a condition which does not occur in nature. Two flaws occur in this given system as the colony expands; first, superposition of junctions is possible and second, the centre of each hexagon is not visited. However, statistical analysis of all angles present in an excavated colony of Alpznza reveals a bias towards angles somewhat lower or higher than 1 20°, the angle between the arms of the Y is 130°, the supporting angles are either 1 loo, 120°, or 120°, 110'. 136 A. D. BELL AND P. B. TOMLINSON Early rhizome generations superficially correspond to a hexagonal pattern, but the bias means that aerial shoots are progressively placed within existing hexagons and there are fewer superpositions. Tesselation is ‘imperfect’, but ecologically, more advantageous. Actual Alpinia clones improve further on the theoretical ideal because a proportion of sympodial units stop growing after initiation so that junctions with a single arm result. Empirical ‘rules of success’ of the arms have been determined by the quantitative study of excavated plants which show that one arm is ‘senior’ to the other, that is, of the two meristems of the pair, one is more likely to succeed. The chance of success of the senior arm is 72%, while that of the ‘junior’ arm is 50% if it is associated with a successful senior arm, but 75%‘if it is associated with a failed senior arm. Given these probabilities, a few double failures occur forming ‘dead ends’ from which there is no forward extension of the rhizome. In nature, most junctions are single-armed, but a proportion of double-armed (Y-shaped junctions) are also present. Production of arms fewer than the theoretical maximum results in an incomplete hexagonal grid with reduced overlap.

Other examples Hexagonal grids occur in unrelated plant families and we have observed them in Gramineae, Nymphaeaceae, and Labiatae as well as in Zingiberaceae, but have not subjected any of the recognized patterns to detailed analysis. An example studied by Smith & Palmer (1976) is Solidago canadensis L. (Compositae), which forms tightly packed clones in late herbaceous stages of succession. The model here is based on the concept of an optimal pattern of stem production which maximizes the site of centrifugal spread, a closed canopy, and minimizes total

Table 1. Examples of species with Y-shaped rhizome systems (from Bell, 1979)

Adenostyles alliarzae Kerner. (Compositae)Jeannoda-Robinson, 197 7 Alpinin ipeciosa K. Schum. (Zingiberaceae), personal observation Bactrzi sp. (Palmae) Smith, A. P., personal communication Bambusa vulgaris Schrad. (Gramineae) Arber, 1934 Carexpida Steudel. (Cyperaceae) Martens, 1959 Dracocephaluin ruyschiana L. (Labiateae) Lukasiewicz, 1962 Dryopterzs robertiana (Hoffm.) C. Chr. (Polypodiaceae) Troll, 1935 Erzophorum anpstifolium Honck. (Cyperaceae) Phillips, 1953 t;lagdhza zndica L. (Flagellariaceae),personal observation Heliconin roitrata Ruiza & Pav. (Heliconiaceae), personal observation Iris sp. (Iridaceae), personal observation Lycopodium luczdulum Michx. (Lycopodiaceae) Primack, 1973 Maranta spp. (Marantaceae), personal observation Mrlocanna baccfera Skeels. (Gramineae) McClure, 1966 Neoregehapauciflora L. B. Smith. (Bromeliacead ‘Halle, Odeman &Tornlinson, 1978 Nuphar lutea (L.1 Sm. (Nymphaeaceae) Chassat, 1962 Nypafruticans Wurmb. (Palmae) Tomlinson, 197 1 Ormunda regalis L. (Osmundaceae) Klekowski, 1976 Pelades albus (L.)Gaerto. (Compositae)Jeannoda-Robinson, 1977 Prlasztes hybrcdus (L.)Gaertn. May & Scherb. (Compositae) Grime, personal communication Ripogonum scandens J. R. et G. Forst. (Smilacaceae) Macmillan, 1972 Sculellarza alpina L. (Labiateae) Lukasiewicz, 1962 Solidago canadensis L. (Compositae)Smith & Palmer, 1976 RHIZOMATOUS PLANTS 157 rhizome length. In the actual system gaps are closed by what are called ‘non- divergent’ rhizomes - those growing in the same linear direction as the parent segment. It is interesting that these authors found that the divergent rhizomes had mean angles of 66.0 k 2.41O (left hand) and 67.6+_2.95O (right hand) that is, closer to the ‘improved’ Y angle of 130° than the ideal tesselating angle of 120’. As in Al,binia, there are other variables which cause the system to diverge from the model, but the authors conclude that there is selection pressure for geometrical order. Examples of Y-shaped rhizome patterns have been described in at least 15 families of flowering plants and ferns (Table 1). However, it is not known if these all result in hexagons.

LINEAR SYSTEMS Zingiberales Medpola and Alpinia may be contrasted because the former has a linear as well as a branching component, while the latter has no linear component. Examples of rhizome systems which are exclusively linear are familiar and occur in aggressive weeds like Agropyron and Pteridium, and are characteristic of certain communities such as sand-dunes (Noble, Bell 8c Harper, 1979) and seagrass meadows. Morphologically, linear rhizome systems are diverse and we deal initially with the Zingiberales, a monocotyledonous order with a diversitv of rhizome morphologies. In the family Zingiberaceae, where the plane of distichv of the rhizome scales is transverse (as in Akinia) there is ‘room’ for a branching component. In Hedychiurn, on the other hand, where the plane of distichv is vertical, lateral tneristeins develop mostly from lower rhizome scales and successive rhizotne segments are predisposed to grow in the same direction as the parent axis. This simple phyllotactic difference would therefore seem to have considerable ecological implication and it is curious that the plane of rhizome distichy separates members of the two major tribes within the Zingiberaceae (Weisse, 1932). At least one species of Heliconia (Heliconiaceae) succeeds in bridging this difference, having exactly the same complement and orientation of meristems as Akinia but only one meristem in a pair normally develops, and it is always to the same side as its parent. Each new branch turns through 60° until it is heading along the straight axis of its predecessors. Other species of Heliconia develop hexagonal grids comparable with those of Alpinia, while in vet others, such as H. imbricata (O.Ktze.1 Baker, despite the transverse distichy, a linear component is made by displacement of meristems. Costus (Costaceae) also has the potential for hexagonal grid formation, but develops in the linear manner because only one meristem of each pair develops and is always positioned on the opposite side to that of its parent resulting in a zig-zag pattern that progresses in a straight line (Bell, 1976). This pattern can be shown to be related to the distinctive phyllotaxv of this genus, most precisely when this value is 1/6. Some species of- Costus, and the related genus Tapeinochilus, escape from this linear constraint by the production of bulbils in the terminal inflorescence which is lowered to the ground in a random direction by the activity of an articulating internode at the base of the aerial shoot. This swollen internode contains collenchymatous mechanical tissue in contrast to the sclerenchyma of all other internodes. 138 A. D. BELL AND P. B. TOMLINSON

A D ------

Proximal end of system Aerial shoot with terminal inflorescence 0 Sterile aerial shoot 0 Solitary inflorescence at ground level 0 Meristem (bud) potentially developing as part of the basic model n Meristem potentially developing to reiterate the model

Figure 4. Branching patterns in the Zingiberales. Diagrammatic plan view based on observed examples. Rhizome segments (lines) and aerial shoots (circles)approximately to scale. A-C. Hexagonal systems (sympodial). A. Simple system, as found in Alpinia speciosa (Zingiberaceae); Heliconia latisjatha Benth. Heliconia rostrata (Heliconiaceae) and Ischnosiphon spp. (Marantaceae). Both renewal buds develop, bifurcating at f 120° to give a hexagonal grid. B. Achasma megalocheilos Griff. (Zingiberaceae); Heliconiapsittacorum L. (Heliconiaceae). As in A but much wider spacing of aerial shoots. C. Unnamed dried specimen (Zingiberales). Paired buds behave alternately as in A and F, i.e., one bud only developing in line ahead, alternating with both buds developing as a + 1 ZOO bifurcation (the location of flowering shoots is not confirmed). D-I. Linear systems. D. Hedychium gardnerianum Rosc. (Zingiberaceae). Buds borne in two ranks, above and below the rhizome, one of the latter develops in line with its parent. All shoots fertile. E. Zzngber officznale (Zingiberaceae), as in D, but shoots either vegetative or fertile. F. Heliconia sp. (Heliconiaceae). Pair of buds situated at the base of each aerial shoot to left and right in the horizontal plane i.e. at right angles to those in D & E (this arrangement is also true of examples GI). Here, only one bud develops, and grows in line with its parent axis. G. Costus cylindricus Jacq. (Custaceae); Heliconia collznszana Griggs. Heliconiaceae. Only one of each bud pair develops, always on the opposite side to that of its parent giving a ‘linear’ zig-zag. H. Costus dinklagei K. Schum. (Costaceae) (after Hall+, 1967). As in G, but the second bud develops into an inflorescence at ground level. I. Aframomum polyanthum (Zingiberaceae). As in G, but the second bud develops into a single aerial shoot. Two additional buds to left and right at ground level develop into inflorescences. J-K. Mixed systems (i.e. part hexagonal, part linear). J. Maranta sp. (Marantaceae). Paired buds behaving as Alpinia (A) to give a hexagonal system plus occasional long branches acting as linear ‘spacers.’ K. Aframomum luteo-album (Zingiberaceae). A monopodial rhizome bearing an apparently unordered sequence of aerial side shoots behaving as AQinia (A)with paired buds, plus occasional sequences of ( 1)-3-(4) inflorescences at ground level. RHIZOMATOUS PLANTS 139 In a numbel- of gingers there is an added element of polymorphism because erect shoots may be either sterile and leafy (assimilating) or flowering but essentially non-assimilating, the most familiar example being the commercial ginger (Zingiber officinale Rosc.). The flowering axes may occupy a precise position in the architecture of the system, as shown for Aframomum polyanthum K. Schum. (Halle, 1967) where there are usually two inflorescences succeeding the two renewal meristems. Aframomum luteo-album K. Schum. and at least one species of Maranta have rhizome patterns combining both the linear and the hexagonal features described above. The diverse branching tactics of the Zingiberales are summarized in Fig. 4 and present a remarkable range of variation. It is significant

F G

Figut-e 5. Examples of rhizome branching patterns in bamboos: plan view with ct-c'ct 5hoots t-cprrwired by double circles, open ends signify the continuation of an axis in a horizontal dirrction (fi~[1111 McClurc. 1966). A. Aambusa pachinensis Hagata. B. Bambusa tuldoides Munro. C. Arundtnarta pusilla A. Cheval .& A. Caniu,.; Chusyuea rcandens Kunth. D. Bambusa vulgaris: Stnarundtnaria nitida (Mitford) Nakai. E. Mrlocanna baccyrra; Schizostachyum hainanense Merrill ex McClure. F. Yushanta niitakayamensls (Havata)P. C. Keng. G. Shibataea kumasasa Makino (Zoll. ex Stend) Nakai. H. Arundinaria tecta Muhl. 1. Phyllostachyi hamhutozdrr. Siebold .& Zuccarini. J. Indocalamus sinks Nakai. K. Chusgueafendlert Munrc~.

10 140 A. D. BELL AND P. B. TOMLINSON that one basic design feature-paired buds at the distal end of each sympodial unit-can give rise to this range of both linear and hexagonal patterns. TO be constructed so similarly and yet be so subtly distinctive implies either the specific development of a precise adaptive geometry in each case, or alternatively that all the patterns are of equal efficiency, which we doubt. This situation is not confined to the Zingiberales, but has been reported in at least two further cases, the bamboos, Fig. 5 (McClure, 1966) and the lycopods, Fig. 6 (Primack, 1973).

Figure 6. Branching patterns in Lycopodtum, modified after Primack (1973). these represent the rhizome system in plan view, the erect shootsi shown in the original have been left out. A. Lycopodium annotinum L. B. Lycopodium lucidulum. C. Lyropodium obsrurum L. D. Lyropodium obicurum, a 'vigorous plant' showing proliferative reiteration.

Carex arenaria L . In many linear rhizome systems, there is departure from strict linearity at infrequent intervals during the process of branching, but there is no obvious adaptive strategy in the system. Carex arenaria L., modelled in Fig. 7 illustrates such a pattern, based on infrequent and irregular branching at an average angle of 15". This is a sand dune plant and one might suggest that such linear systems are appropriate to a mobile substrate which itself forms narrow bands. However, the same explanation cannot account for seagrasses. Seagrasses, in fact, illustrate one further principle of rhizome geometry which needs detailed consideration.

Seagrass rhizomes Marine angiosperms are wholly rhizomatous and develop extensive meadows by vegetative spread. They therefore offer an unusual opportunity to study the significance of rhizome geometry, especially as they are highly dependent on the continuous activity of vegetative meristems, dormancy of meristems being absent from subtropical and tropical examples. Extensive genets may exist, as suggested RHIZOMATOUS PLANTS

Carex arenoria

Figure 7. (;arc\ nrfi~nrin(Cyperaceael. Plan view of an 8 year old rhizome generated hv compiitcr on ttir b\is 01 ot>\ewcdexamples.

by large populations of one sex in dioecious species such as Syringodium (Cymodoceaceae). The degree of specialization of the shoot system varies (Tomlinson, 19 74). In less specialized examples, such as Enhalus, Posidonia, Zostera, Cymodocea and Halodule, branching does not follow any obvious predictable pattern (Fig. 8). In more specialized examples such as Amphibolis, Thnlassodendron and Syringodium the architecture includes no branching component, the syrnpodium is strictly linear and does not proliferate the system (Fig. 8). Proliferative branching is entirely reiterative and results from damage to the rhizome, or from some environmental disturbance which causes reserve meristems to develop (in Amphibolis) or induces some phase change so that rhizome shoots develop from erstwhile leafy shoots (in Syringodium). Thalnssia is one of the most highly organized of the seagrasses, but can only proliferate rhizome meristerns indirectly and without any regular pattern (Tomlinson & Vargo, 1966). No detailed studies which provide statistical information about the proliferative capacities of seagrasses have been made. From this it can be concluded that it is the latent meristem population carried by many linear .~-. rhizomatous plants that governs their potential productivity (e.g., Tomlinson, 1974; see also Appendix Section L). Foliageleaves, inflorescences, meristems(erect and

II II

IJII Scale leaves, meristems 4 -4-/ (erectshoots), roots Enholus and Posidonio Tholossodendron Monopodial,foliage leaves Foliageleaves, meristems Sympodial, scole leaves (erectshoots with inflorescences; rhizomes), I II roots inflorescences, I I I ? Zoslero II II I Monopodial, foliageleaves P I Foliage leaves, I W inflorescencesor m flowers,meristems r Syringodium r II (long- and short-shoots) II Monopodial,scale leoves P 1- z 1( 1 Foliage (2) scale 1 I1 I. tr / leaves,flowers, Cymodoceo and Hofodufe meristems(Img- and I meristems(lateral Monopodial,foliage leaves short-shoots), roots ____--- -- ( sec Holophilo) (I) Scale (2)foliage Foliage leaves,flowers, I ,Foliage leoves meristems (erectand I horizontalshoots) CI II IJ Holophilo (sec Americanae) Scale leaves,meristems Monopdial,scale leaves (lateralshoots or Amphibolis rhizomes), roots -Sympodial, scaleleoves

Foliageleaves Foliageleaves, meristems I \I 1 (rhizomes),flowers, I roots Key I I -+ Indeterminate I Determinate(or short-shoot) ;m, * Scale leaves, meristems I Tholossio Monopdial,scale leaves \ (short-shoots),roots I RHIZOMATOUS PLANTS I43

SHOOT DIMORPHISM One of the characteristic features of seagrasses is the dimorphism between leafy erect shoots and horizontal scale-bearing shoots which occurs in Amphibolis, Syringodium, Thalassodrndron and reaches its highest development in Thalassia. This shoot dimorphism is also found in many terrestrial rhizome systems and may complicate a geometrical pattern or elaborate a linear system !€‘rat, 193,5’; Mueller, 1941; Webster 8c Steeves, 1958; Persikova, 1959; O’Brien, 1963). Primack (1973) has shown, for species of Lycopodium in eastern North America, that annual increments are established according to precise disposition between erect leafy photosynthetic shoots and horizontal creeping shoots, and that the dimorphism does not involve any marked contrasts in microphyll morphology. In Fig. 6 we have simplified the original diagrams by omitting the erect shoots in order to show the basic geometry. Some Lycopodium species with a pronounced linear strategy of growth proliferate their rhizomes onlv in an opportunistic manner. In bamboos there is some evidence (Takenouchi, 1932; McClure, 1966) that long and short units may be coupled in a pattern utilizing two different angles. Figure 9 shows a constructional unit in which long shoots Gr a series of short shoots, long shoots in turn arising from the distal short shoots of a previous generation. Angles of 60° and 45” are combined to give net divergences of 45O and 15O, as indicated. When these ideal systems are expanded as populations by ‘simulation, the patterns represented in Fig. 9 are generated, with the predominant exploratory movement tightly to the left. This system shows well the idherent capabilitv of the octagonal pattern on which it is based (Fig. 10).Based on McClure’s data (see Fig. 5) an intricate system, but with little order, can be synthesized. The significance of such systems can only be appreciated by extensive excavation and analysis of existing systems, with appropriate statistical analysis of measured parameters. For bamboos this still remains to be done. The relation between rhizome morphology and reproductive strategy in bamboos is illustrated by the study of Phyllostachys bambusoides Siebold & Zuccarini by Numata, Ikusima 8c Ohga (1974). They showed that gregarious flowering is preceded by the development of specialized basal regenerative branches, which persist after the parent culm has died. These regenerative shoots add a further dimension to the life history strategies of bamboos since they show that such plants are not strictly monocarpic, as is usually maintained (Janzen, 1976).

FACTORS INFLUENCING PATTERIV A number of other Factors may mask the underlying constructional organiza- tion. Physiological depth control mechanisms have already been mentioned. In addition it has been shown that certain rhizomatous plants have a variable

Figurc 8. Rhimine systems in seagrasses (marine monocotyledons) after Tomlinson f 19741, shown diagi-amrnaricall~,in rzdp \iew. All are linear systems and proliferative branching apparently lackc any geornetriral precision. In the diagrams arrows represent indeterminate meristems; axes ending in determinatc meristern> ai-e shown as dotted lines; in all systems these are erect. The kinds of appendages produced bv each type of meristem is shown in the boxes to the left. Numbers 1-eprrsent the internodes between ;uccessive units along the rhizome. 144 A. D. BELL AND P. B. TOMLINSON

c RHIZOMATOUS PLANTS 145

E’iguw 10. Plan view of a more elaborate rhizome system based on McClure’y forms Ccf Fig. 5) branching response to differing environmental conditions (Hutchings & Barkham, 1976; see also Appendix Section M). Conversely, and possibly more frequently, the morphological behaviour will remain constant in variable conditions, although this is rarely tested (Anderson, 196 la). Conservatism may be of a temporary nature (e.g., O’Brien, 1963; see also Appendix Section N), or may eventually give way to an evolutionary change (e.g., Klekowski, 1976; Klekowski & Berger, 1976; see also Appendix Section 0). The natural mobility of a ramet can be overshadowed by the effect of prevailing wind, with most susceptible plants moving naturally down wind (Hansen, Dayanandan, Kaufman & Brotherson, 1976; see also Appendix Section PI, but occasionally upwind (Luff, 1965). Another aspect of variable rhizome behaviour is the phenomenon of ageing, represented by phases of growth within a clone; rhizomes in the old part of a clone may behave differently from rhizomes in the vanguard (Watt, 1970; see also Appendix Section Q). However, the longevity of many clones (see earlier) would seem to preclude this ageing phenomenon. 146 A. D. BELL AND P. B. TOMLINSON Interaction between plants will modify the pattern. Different parts of a single ramet, or genet, or even parts of different genets may form mutual clumps, establishing aerial shoots at discrete locations even in apparently uniform environments (Greig-Smith, Gemmel 8c Gimingham, 1947 ; see also Appendix Section R). Conversely a competitive situation can lead to the establishment of invasive tactics (Watt, 1955; see also Appendix Section S).

COMPUTER SIMULATION We mentioned earlier the use of simulated rhizome growth patterns generated by computers which have a visual display as a means of assessing long-term effects of population expansion by ramets (Bell, 1979b). The topic has been explored in a preliminary way by Bell (1976)on the basis of known examples. Of particular value is the continuous recording of growth patterns by means of frame- by-frame cint. photography of a pattern projected on a screen, so that extended population behaviour can be displayed rapidly and visually when run subsequently in a projector at normal speeds. This approach allows prediction to be made about the extent and density of clonal populations in the future, and provides detailed information concerning the proximity and movement of ramets in the short term. It also allows an assessment to be made of the effect on a plant’s performance of varying the branching parameters. Simulation could eventually provide a rapid method of assessing competitive interaction, as when two rhizome populations based on different patterns, are ‘grown’ together in the same program. This could be used, for example, to estimate interplay between crop and weed. Such programmed confrontations have not yet been devised. An interesting extension of such a design would be the estimation of productivities and a check on reproductive mechanisms-selection for prolific flowering in a rhizomatous plant might lead to a reduction in the number of reiterative meristems present and an overall reduction of productivity in the long run. It is obvious that such applications are dependent on a knowledge of the behaviour of rhizome systems in nature. This would include an assessment of the architectural potential of a rhizomatous plant, a statistical analysis of its actual behaviour, along the lines of the study ofSolidago by Smith & Palmer ( 19761, and a study of growth responses in different habitats.

CONCLUSIONS It seems reasonable to assume that the same selection pressure which has induced the rhizomatous habit has also maximized the adaptive geometry of the resulting pattern. The diversity of rhizome patterns which we have begun to explore seem accountable by this simple principle. Such an approach to organism shape is well established in the realms ofzoology (Stahl, 1962; Raup 8c Michelson, 1965; Braverman & Schrandt, 1966; Raup, 1966, 1967, 1968; Ede & Law, 1969; Oxnard, 1969; Raup 8c Seilacher, 1969; Gould, 1970). We have confined ourselves to the adaptive architecture of rhizomes as a two dimensional test case, and while emphasizing the importance of branching patterns we have indicated how these may be obscured by circumstances and therefore pass unnoticed. The relationship between the branching of a plant and RHIZOMATOUS PLANTS 147 the environment is nevertheless quite fundamental, and we are extending our studies to a variety of plant types, especially trees, relating the morphological details of their developmental growth to the establishment of a three dimensional invasion of space i.e. crown interactions in a canopy. This field has been pioneered by Fisher 8c Honda (1978).

ACKNOWLEDGEMENTS This study was made possible by the award of a Science Research Council (London)Fellowship to A. D. B. and was begun while he was a Cabot Foundation Post-doctoral Fellow at Harvard University. Permission by the editors of the Journal of' the Arnold Arboretum and the Harvard University Press, to reproduce Figs 1 and 5 respectively, is gratefully acknowledged, as is the assistance of Marion Wade-Evans.

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HIBLIOGRAPHICAL APPENDIX

A Root bud, Tainin, 1956 Rogers, 1928 Canfield, 1957 Rnuh, 1937 Penzes, 1958 Weher, 1937 Chadwick, 1960 Korrnnntk & BIIl\\Ii, 1967 KershaLv, 1960 Petel SO11 & TholIlds, 197 1 Rabotnov. 1960 Peterson, 1975 Harherd, 196 1 Harberd, 1962 B. Clone rhap Pbnzes, 1963 Mar tens, 193’) Oinonen, 1967 a,b,c Watt, 1947 Barroiv, Costin & Lake. 1968 Kci ~li~i~,19 50 Oinorien, 1968 Fedor ov, 1966 Pigott. 1968 Austin, 1968 Oinonen, 1969 Pigott, 1968 Bouchard & Maycock, 1970 Znugolnova, 1974 Cartlcdge & Carnahan, 197 1 Rabotnov, 1975 Flower-Ellis, 197 I Bell, 1976 Oinonen, 197 1 Tarnni, 1972 a,h

C. Clone: innximuin site E. Traumatic reiteration Whit ford, 1949 Schwartz, 1923 Ovington, 1953 Kadainbi, 1949 Webb, 1954 a. t) Ueda, 1960 Webb, 1958 Barker & Collins, 1963 de Byle, 1964 Charles, 1964 Barnes, 1966 Silshu?, 1964 Harherd, 1967 Fishrt- & Toinlitison, 1972 Barnes, 1969 Jewiss, 1972 Harherd & Orven, 1969 Bell, 1974 Wall, 1971 Lace?, I974 Stenekrr, 1973 Bell, 1979 a

D. Clonc~age F. Adaptiiv rezteratzon Flamn, 1922 Etter, 1951 Anderson & Dichl, 1932 Johnson & Bucttholtz, 1957 Moliuch, 1938 Davies & Laude, 1964 Camp, 194 1 Fiala, Dykyjova, Kuet & Svoboda, 1968 Darrow & Catrip. 1945 Pigott, 1968 Tainni, 1948 Westlake, 1968 Eplirig & Lewis, 19.52 Fiala, 1970 a,b Pelton, 1953 Tomlinson, 1974 Cottam, 1954 Silva, 1976 Moldenke, 1955 Noble, Bell & Harper, 1979

11’ 158 A. D. BELL AND P. B. TOMLINSON

G. Merzstem position in relation topattern J . General accounts of morphological pattern Massart, 1903 a,b Holm, 1891 Veh, 1930 Velenovsky, 1890 Weisse, 1932 Miiller, 1894 Cooper, 1951 Maige, 1900 Phillips, 1952 Hauri, 1912 Palmer, 1954 Sherff, 1912 Palmer, 1958 Monoyer, 1929 Gillet & Tinchant, 1964 Evans & Ely, 1935 FisherJ. E., 1972 Meusel, 1935 Bell, Roberts & Smith, 1979 Troll, 1935 Conway, 1936 Martens, 1939 H. Response to immediate environment Weber, 1950 Riinbach, 1899 Bogdan, 1952 Emerson, 192 1 Caldwell, 1957 Laing, 1941 Goodman, 1957 Clapham, 1945 Persikova, 1959 Bennet-Clark & Ball, 195 1 Goodman, 1960 Palmer, 1955 Ikehata & Tsuboi, 1961 Palmer, 1958 Subra & Guillemot, 1961 Ormond, 1960 Chassat, 1962 Fisher, 1964 Lukasiewicz, 1962 Wareing, 1964 O’Brien, 1963 Marshall, 1965 Galil, 1968 Pfirsh, 1965 Pigott, 1968 Pfirsh, 1966 Haslam, 1969 Watt, 1969 I. Precise accounts of morphologtcal pattern Fisher, J. B., 1972 Celakovsky, 1881 Lacey, 1974 Miki, 1927 Meusel & Kastner, 1974 Fritsche, 1930 Sobey & Barkhouse, 1977 Gill, 1933 Hagemann & Schulz, 1978 Watt, 1940 Walters, 1950 K. Rhizome studies lacking morphologtcal detail Phillips, 1952 White, 1808 Phillips, 1953 Vochting, 1889 Caldwell, 1957 Raciborski, 1894 Ueda, 1960 Bayer, 1904 Franqois, 1964 Pamrnel & Fogel, 1909 McClure, 1966 Nishirnura, 1922 HallC, 1967 Darrow, 1929 Austin, 1968 Porterfield, 1930 Charlton, 1968 Veh, 1930 Lorougnon, 1969a Kephart, 1932 Lorougnon, 1969b Takenouchi, 1932 Espagnac & Luck, 1970 Weisse, 1932 Tomlinson, 1970b Evans & Ely, 1933 Serebryakova, 197 1 Tidmarsh, 1939 Macniillan, 1972 Smith, 1941 Primack, 1973 Webb, 1941 Bell, 1974 Ovington, 1947 Tomlinson, 1974 Tamm, 1948 Tornlinson & Esler, 1973 Etter, 1951 Bezdeleva, 1975 Etter, 1953 Shah & Raju, 1975 Reznichenko, 1957 Jeannoda-Robinson, 197 7 Palmer, 1958 Bell, 1978 Dasanayake, 1960 Callaghan, 1978 Goodman, 1960 RHIZOMATOUS PLANTS 159

Licth, 1960 Anderson, 196 I a,b Rivals, 1960 Kershaiv, 1962 a,b Bowcs, 196 1 Snagovskaja, 1966 Morez & Guillernot, 1961 Wilson, 1968 Berg, 1962 Steshcnko, 197 1 Kershaw, 1962 a,b Matveev, 1972 Tondinson, 1962 McNaughton, 1975 Langer, 1963 Shea, Warren & Nirring, 1975 de Bvle, 1964 Hutchings & Barkhain, 1976 Onyekwelu, 1966 Falinska, 1977 Chabot-Jacquety, 1967 Donskova, 1968 f.ark morphological response to (I variable Cali(, 1968 rl'. environment Davics, 1970 Massart, 1903 a,b Haslani, 1970 Ernerson, 1921 Jeune & Cuswr, 197 1 Evans, 1927 Rawal & Hai-dan, 197 1 Birse, 1957 Tonilinson. 197 1 Girningharn & Bine, 1957 Fnnshawe, 1972 Birse, 1958 Horovitz& Galil, 1972 Palrnei-, 1962 Anderson & Louc-ks, 19 73 Snaydon, 1962 Gorhairi & Soiners, 1973 O'Brien, 1963 Horovirz, 1973 Ginzo & Lovell, 1973 a,b Sarukhin & fini-pei-, 1973 Abrahanison, 1975 a,h Brasleigh & Yarrington, 1974 Bernard & MacDonald. 1974 Bernard, 197,; 0. Evoliihonarz. chang? McKendrick, Clmton. Owensby & Hyde, Sherff, 1912 1975 Aston & Bradshaw, 1966 Calhghari, 1976 Jain & Bradshaw, 1966 Mitsuta. 1976 Harris, 1970 Jain, 1972 L. f'roducfwity in relation to rneristem performance Holland, 1974 Cooper, 19.5 1 Spencer, Hely, Govaars, Zorin & Goodi~iaii,19 5 7 Hamilton, 1975 Iwaki & Midoi-ikawa, 1968 Wu, Bradshaw8c Thurnian, 1975 Tom linson , 1Y 7 4 Klekowski, 1976, Persson, 1975 Klekow5ki & Berger, 1976 Callaghan, 1976 Turkington & Harper, 1979 a,b Callaghan, 1977 Callaghan &Collins, 1976 P. .Mobilitl due to wind Walton, 1976 Burges, 1951 Sohn & Policansky, 1977 Agnew & Hainrs, 1960 Noble, Bell & Harper, 1978 Lieth, 1960 Tierema & Vi-ornan, 19 7 8 Agnmv, 1961 Harpei- & Bell. 1979 Luff-, 1965 Bari-ow, Costin & Lake, 1968 M, Morphological rerponv to a variable environment Hansen. Dayanandan, Kaufinan & Jefferies, 1916 Brotherson, 1976 Watkins, 1940 Smith, Nielson & Ahlgi-en, 1946 Q. Ageing Phillips, 1952 Watkins, 1940 Phillips, 1953 Watt, 1945 Phillips, 1954 Watt, 1947 Millikan, 1957 Phillips, 1953 Krrshaw, 1958 Phillips, 1954 Bradshaw, 1959 Persikova, 1959 Bradshaw, 1960 Goodman, 1960 Kershaw. 1960 Kershaw, 1960 160 A. D. BELL AND P. B. TOMLINSON

Anderson, 1961a,b Kershaw, 1963 Watt, 1970 Onyekwelu, 1966 Cartledge & Carnahan, 19 7 1 Wall, 1971 S. Invasive tactics Antonovics, 1972 Mueller, 194 1 Egorova, 1972 Salisbury, 1942 Zaugohova, 1974 Bogdan, 1952 Ovington, 1953 R. Mutual clumping Phillips, 1953 Greig-Smith, Gemmel & Gimingham, Phillips, 1954 1947 Watt, 1955 Holdgate, 1955 Donald, 1963 Kershaw, 1958 Tripathi & Harper, 1973 Bormann & Graham, 1959 Silva, 1976 Kershaw, 1962 a,b Soane & Watkinson, 1979