Annals of 80: 571–582, 1997

REVIEW ARTICLE

The Fundamental Relevance of and to Research

ROLF SATTLER and ROLF RUTISHAUSER Department, McGill UniŠersity, Montreal, Quebec, Canada H3A 1B1 and Institut fuW r Systematische Botanik und Botanischer Garten, UniŠersitaW tZuWrich, Zollikerstrasse 107, CH-8008 ZuW rich, Switzerland

Received: 21 August 1996 Accepted: 3 June 1997

Plant morphology, including morphogenesis, remains relevant to practically all disciplines of plant biology such as molecular , , , evolutionary biology and systematics. This relevance derives from the fact that other disciplines refer to or imply morphological concepts, conceptual frameworks of morphology, and morphological theories. Most commonly, morphology is equated with classical morphology and its conceptual framework. According to this, flowering and certain other taxa are reduced to the mutually exclusive categories of , stem (caulome) and (phyllome). This ignores the fact that has undergone fundamental conceptual, theoretical and philosophical innovation in recent times. These changes, when recognized, can fundamentally affect research in various disciplines of plant biology. They may even change the questions that are asked and thus may affect the direction of future research. If, for example, plant diversity and are seen as a dynamic continuum, then compound can be seen as intermediate between simple leaves and whole . Recent results in molecular genetics support this view. Phylogenetically, this could mean that compound leaves are the result of developmental hybridization, i.e. partial . Many other examples are given to illustrate the relevance and potential impact of basic conceptual and theoretical innovations in plant morphology. # 1997 Annals of Botany Company

Key words: Plant morphology, plant morphogenesis, molecular plant genetics, developmental genetics, , , evolutionary plant biology, plant systematics, cladistics, continuum morphology, process morphology, process philosophy, perspectivism, complementarity, homeosis, homeotic mutants, developmental hybridization, developmental mosaics, , metamerism.

recognize, of course, that external and internal form are INTRODUCTION intimately related. The purpose of this paper is two-fold: (1) What is plant morphology? Literally, the term ‘mor- to show that morphological concepts are used or implied in phology’ is derived from two Greek : morphe, which all major disciplines of plant biology such as genetics, means form and\or structure, and logos, meaning discourse , physiology, ecology, systematics, evol- or investigation. Thus, plant morphology is the investigation utionary biology, etc. Therefore, these disciplines are more of plant form and\or structure. This can be interpreted in or less influenced by morphology; and (2) to show that the either a narrow or a broad sense (e.g. Sattler, 1978). In the disciplines of plant biology are affected to some extent by narrow sense, morphology refers only to external form (see, progress in plant morphology which comprises new em- for example, Bell, 1991). In the broad sense, it comprises pirical data, new concepts and conceptual frameworks, and form and structure at all organizational levels, i.e. the form new ways of thinking. Whereas the relevance of new em- and structure of whole plants, organs, tissues, cells, pirical data is generally recognized, theoretical and philo- , molecules, etc. Thus, morphology sensu lato sophical innovations are often overlooked. Many plant includes and even structural biochemistry. biologists believe that the basic conceptual framework and Regardless of whether morphology is defined narrowly or way of thinking of morphology were well established in the broadly, it deals with the change of form during time, 19th and early 20th century. Therefore, it is usually taken during and phylogeny. Since morphogenesis is the for granted, that if reference to morphology is necessary, it development of form, especially during ontogeny, mor- must be in terms of classical morphology, i.e. in terms of the phology comprises morphogenesis. We included ‘morpho- categories root, stem, and leaf for most higher plants. Most genesis’ in the title of this paper for two reasons: firstly to textbooks and other publications reinforce this belief make it clear that we do not understand morphology in an because they tend to ignore more recent theoretical and extremely narrow and static sense according to which it philosophical innovations. Thus, the student is misled to would refer only to mature form or structure, and secondly think that fundamental progress in morphology has come to to emphasize that the dynamics of form and structure are of an end. special concern to us. However, there have been major theoretical and philo- The emphasis in this paper will be on plant morphology sophical innovations during last 30 years or so, some of the sensu stricto, i.e. external form as it changes during time. We most fundamental of which include: (1) the introduction of

0305-7364\97\110571j12 $25.00\0 bo970474 # 1997 Annals of Botany Company 572 Sattler and Rutishauser—ReleŠance of Morphology the Lindenmayer languages or algorithms (L-Systems) (e.g. variate analysis (Jeune and Sattler, 1992). In this dynamic Lindenmayer, 1968, 1978) culminating in Prusinkiewicz’ continuum, the process combinations that we call typical computer simulations of plant form and development (e.g. roots, shoots, stems, leaves and are linked by Prusinkiewicz and Lindenmayer, 1990); (2) the development intermediate process combinations that share processes of of fractals, chaos theory and nonlinear dynamics and its the typical structures to various degrees. application to the study of plant form (e.g. Mandelbrot, All of the above fundamental innovations (and others 1982; Barabe! , 1991; Peitgen, Jurgens and Saupe, 1992; that have not been mentioned) can have an impact on Kaandorp, 1994; Corbit and Garbary, 1995; Oldeman and research in the various botanical disciplines that rely on Vester, 1996); (3) the elaboration of the metameric and morphological concepts. Since it is beyond the scope of a modular concept and the idea of the plant as a metapopu- single paper to examine the impact of all major innovations lation facilitating the integration of morphology and of the past decades, we shall focus on the relevance of the population biology (White, 1979, 1984); (4) the analysis of notion of the dynamic continuum, i.e. the continuum view plant architecture in terms of a continuum of architectural of plant form and process morphology. However, we shall models (Halle! , Oldeman and Tomlinson, 1978; Edelin, not totally ignore other innovations. 1991; Oldeman and Vester, 1996); (5) the elaboration of Process morphology and other fundamental innovations perspectivism (general principle of complementarity) ac- affect not only the outcome of research in other fields but cording to which contrasting or contradictory models (or may even change the questions that are asked and thus conceptual frameworks) are complementary (not antag- influence the direction in which research proceeds (Sattler, onistic) to each other (see Rutishauser and Sattler, 1985, 1990, 1993). For example, instead of asking ‘Is it this or 1987, 1989). An example is the complementarity of the that?’, one would ask ‘How is it related to this or that?’ classical model (according to which the consists of (this or that being other processes or process combinations). stem(s) and leaves) and the metameric model that constructs Thus, a categorical world view is superseded (or at least the whole shoot of metamers only (Rutishauser and Sattler, complemented) by a dynamic relational view. If, in addition, 1985: Table 1 and below); (6) the rediscovery of homeosis it is recognized that relations are not only external but also which has led to an increased integration of molecular internal, this has further consequences that have been genetics and morphogenesis (see, for example, Meyen, 1973, elaborated by various process thinkers (e.g. Cobb, 1988; 1987; Cusset, 1982; Sattler, 1988, 1994; Rutishauser, 1989, Birch, 1990). 1993; Coen, 1991, Meyerowitz, 1995). Homeosis also fundamentally affects the notion of homology (Sattler, 1988, 1994; see point (8) below; (7) the elaboration of a continuum view of plant form (Sattler, 1974) and its GENETICS, MOLECULAR BIOLOGY AND confirmation by multivariate analysis (Sattler and Jeune, MORPHOLOGY 1992; Cusset, 1994). Philosophically, this view is based on, Genotype and phenotype or compatible with, fuzzy logic and fuzzy thinking (Kosko, 1993): the world is not only seen in terms of ‘either-or’, Traditionally, genetics deals with the relationship of black or white, this or that, but in terms of ‘more or less’ of genotype to phenotype, to traits, and their inheritance. which the ‘either-or’ becomes a special extreme case. Thus, The phenotype and its traits are often morphological Aristotle’s basic logical law ‘A or not-A’ is superseded (see characters such as stem length, flower site, form. Thus, Kosko, 1993; for applications in see morphology and morphological concepts play an important Rutishauser, 1995); (8) the development of the notion of role in genetic analysis. This has been so from the beginnings partial homology (Sattler, 1966; Meyen, 1973) and the of genetics to the present time. Mendel elaborated the quantification of homology relations of plant form (Jeune fundamental principles of genetics using morphological and Sattler, 1992; Sattler and Jeune, 1992); (9) the traits of the garden pea. Although modern workers elaboration of ‘process morphology’ according to which investigate molecular traits in addition to morphological form or structure are seen as process (Sattler, 1990, 1992; ones, the latter are still widely used because we want to Sattler and Rutishauser, 1990; Jeune and Sattler, 1992, know how morphological traits are related to the 1996; Hay and Mabberley, 1994; Mabberley and Hay, and how they are inherited. Gottlieb (1986), in an article on 1994; Mabberley, 1995). This contrasts with the traditional ‘The genetic basis of plant form’, discussed the relationship approach in which form or structure are seen as the result of between genetics and morphology. In an earlier publication process which implies that there are processes on the one on ‘Genetics and morphological evolution in plants’ hand and forms or structures on the other. According to (Gottlieb, 1984), he emphasized the evolutionary aspect in process morphology there is only process. Thus, structure is genotype-phenotype relations which implies inheritance. It process or, more specifically, a process combination. is obvious that in many studies of inheritance morphology Similarly, diversity of structures is a diversity of process continues to play an important role. For example, a more combinations while morphological evolution is change of recent article by Shaw and Hansen (1993) dealt with ‘The process combinations during ontogeny and phylogeny inheritance of vegetative growth traits in strawberries (Sattler, 1990, 1992, 1993). (Fragariaiananassa) grown at low temperatures and their The continuum view of plant form and process mor- relationship to field productivity’. Regardless of the special phology has been integrated, thus leading to the notion of a focus and context of the genetic research, morphological dynamic continuum which has been confirmed by multi- concepts form an integral part. Sattler and Rutishauser—ReleŠance of Morphology 573 relevant to ask how the of tendrils (such as those of Mutants, molecular genetics and deŠelopmental genetics peas) relate to those of stems. The molecular elucidation of mutations has become very Leaves share developmental processes with stems. In important. Nonetheless, we remain equally interested in the Chisocheton and Guarea (Meliaceae) there are compound mutants that are produced by the mutations. These mutants leaves that show indeterminate growth combined with often affect the morphology of plants. Hence, they are seasonal growth increments due to an apical at the described in morphological terms. Examples are mutants in leaf tip (Fisher and Rutishauser, 1990; Miesch and Barnola, Pisum, the garden pea, such as tl (claŠicular or tendril-less), 1993). Thus, such ‘leaves’ share developmental processes st (stipules reduced), and af (afila) in which leaflets are with distichous shoots. Each flush of young leaves at the replaced by tendrils (e.g. Marx, 1987; Gould, Cutter and shoot tip is temporarily correlated with the flush of young Young, 1994). pinnae at the end of compound ‘leaves’. Even more typical Mutants, especially homeotic mutants such as those of compound leaves share processes with shoots (Sattler and and Antirrhinum, play an important role in Rutishauser, 1992; Lacroix and Sattler, 1994; Rutishauser molecular and developmental genetics (e.g. Coen, 1991; and Sattler, 1997; see also Jackson, 1996). Rutishauser, 1993; Bowman, 1994; Meyerowitz, 1995). Not only traditional morphologists, but also molecular Although the emphasis may be on molecular mechanisms, biologists have difficulties defining the term ‘leaf’ in morphology remains relevant. Eventually, we want to dicotyledonous plants (Tsukaya, 1995). If they are to explain the development of organisms of which mor- understand the leaf, they must analyse leaf-specific muta- phogenesis is a central aspect. tions. However, the leaf axis ( and rachis) and the shoot axis (stem) may show a certain degree of devel- opmental similarity. For example, some mutants of Arabi- ReleŠance of continuum and process morphology dopsis exhibit the same defect in the petiole and in the stem In genetic and molecular studies, reference to morphology (Tsukaya, 1995). According to Tsukaya et al. (1993), the is usually in terms of classical morphology (the root, stem, acaulis 2 (acl2) mutant has a defect in the elongation of the leaf framework), as if classical morphology were the only inflorescence axis, the flower stalks (pedicels) and the leaf conceptual framework that exists. Gottlieb’s (1986) dis- petiole, but leaf blades are of normal size. Therefore, cussion of the genetic basis of plant form is one of the few Tsukaya (1995) concluded that the petiole should be exceptions where an alternative to classical morphology is considered an axial . This view corroborates ideas considered from a genetic point of view. Gottlieb refers proposed by Rutishauser and Sattler (1985, 1997): the axial specifically to the concepts of the metamer and plant organs of leaves are petioles and rachides, whereas the axial metamerism. However, when he describes mutants, this organs of shoots are stems, including peduncles and pedicels description is in terms of classical morphological concepts within inflorescences. All these axial organs have some such as internode, leaf and parts of the leaf, because developmental processes in common. New findings in traditionally geneticists have related genetic changes to molecular and may support the view units of classical morphology. It would be interesting to that certain developmental traits in leaves and stems know how mutations may affect whole metamers or other (shoots), are related to a set of endogenous factors that are non-conventional units such as phytons and phyllomorphs identical in both leaves and stems (shoots). (e.g. Jong and Burtt, 1975; Rosenblum and Basile, 1984; As pointed out already, morphology also plays an Rutishauser and Sattler, 1985). important role in molecular research on floral homeotic Vienne and Gottlieb (1990) investigated proteins in leaves mutants of Arabidopsis and other taxa (e.g. Coen, 1991; of wild-type and homeotic mutant morphs of pea. In a Coen and Carpenter, 1993; Meyerowitz, 1995). In most, if comparison of 686 proteins in stipules, leaflets and tendrils, not all, of this work, reference is made only to classical they found only seven quantitative differences between morphology, i.e. the mutants are described in classical leaflet and tendril, and none between leaflet and stipule. terms. Coen and Carpenter (1993) state this explicitly. These results are clearly described in terms of classical According to classical morphology, a flower is a modified morphology according to which stipules, leaflets and tendrils monaxial, determinate shoot whose appendages such as are parts of the leaf which as a whole structure is , , and carpels are homologous to leaves fundamentally different from the stem and the root. In what (e.g. Goethe, 1790; Weberling, 1989; Coen and Carpenter, sense is continuum and process morphology relevant to the 1993). Besides this common view, there are other interpre- perception of these results and their interpretation? It tations and descriptions of flowers (e.g. Croizat, 1960; 1962; would not change the results, but would place them into a Melville, 1962; 1963; Sattler, 1965, 1988; Macdonald and different perspective which would lead to different questions Sattler, 1973; Meeuse, 1986, 1990; Leroy, 1993; Lo$ nnig, and consequently to a different direction of subsequent 1994; Burger, 1996). Even Goethe, who is often considered research. From the continuum point of view, the stem is not the founder of classical plant morphology, entertained fundamentally different from the leaf because stems and alternative views (see, for example, Rutishauser and Sattler, leaves are linked through intermediate forms such as tendrils 1985: Table 1). For example, he acknowledged ‘the fertility (Sattler and Jeune, 1992). Tendrils share some devel- which is latent in the leaf’ [Arber’s (1946) English translation opmental processes such as radial growth with typical stems of Goethe’s (1790) essay] which implies that the leaf, (e.g. Gould and Cutter, 1986; Meicenheimer et al., 1983; including floral appendages, has the potential to form Cote! et al., 1992; Gould et al., 1994). Therefore, it would be (es) (Dickinson, 1978). Others, such as Croizat and 574 Sattler and Rutishauser—ReleŠance of Morphology Meeuse, diverged further from the classical flower concept biology, but also relate to the general theoretical framework and claimed that not all flowers are homologous with each of these disciplines. This relationship may be illustrated with other because some of them are monaxial whereas others regard to heredity. Heredity is generally understood to be are polyaxial. Thus, comparing a monaxial flower with a the result of the passing on of genes, i.e. material particles polyaxial one would be like a comparison of a classical which contain the hereditary information. This particulate flower with an inflorescence. According to Motte (1944, view of heredity has been criticized by process-oriented 1946), Melville (1962, 1963) and others, the flower of the biologists. A process view of heredity has been suggested as Brassicaceae (Cruciferae) is a polyaxial system. From the an alternative (Ho, 1988; Oyama, 1988, 1989). According to point of view of continuum and process morphology, this view, ‘heredity—a name given to the observed constancy monaxial and polyaxial systems are no longer mutually of reproduction—must ultimately be looked upon as a exclusive categories; rather a dynamic continuum can be process, and not as some material which is passed on from envisaged between them, i.e. between inflorescence and parent to offspring’ (Ho, 1988). This means that heredity (monaxial) flower (e.g. Rutishauser and Sattler, 1985; resides in the complex interrelations of processes that Sattler, 1988, 1992, 1994). Some of the homeotic mutants comprise the organism–environment system. Morphogen- such as the floricaula ( flo) mutants of Antirrhinum investi- etic process combinations, the focus of process morphology, gated by molecular geneticists appear to support this view are integral aspects of the whole dynamic system. Thus, (Coen and Carpenter, 1993) and naturally occurring taxa process morphology is intimately related to the process view also confirm it (e.g. Sattler, 1988, 1992; Leroy, 1993). One of heredity, which in turn has broader ramifications such as reason, largely overlooked by molecular geneticists, for why the transcendence of -centred biology and the nature\ flowers of many taxa are more or less intermediate between nurture dichotomy (e.g. Ho, 1988; Oyama, 1989; Gray, a monaxial and polyaxial system is because individual 1992; Hubbard and Wald, 1993; Goodwin, 1994; Holdrege, stamens or fascicles (superposed to petals in several 1996). taxa) are more or less intermediate between a phyllome and a branchlet (Rutishauser and Sattler, 1985). Sattler and PHYSIOLOGY AND MORPHOLOGY Jeune (1992) demonstrated this relationship quantitatively using principal component analysis based on eight structural Physiology deals with the functioning or activity of plants and developmental parameters. For example, the stamen of and how it is affected by various factors such as minerals, Comandra umbellata is almost halfway between a typical hormones and genes. Since many of these factors also phyllome (leaf) and a typical caulome (stem), i.e. its distance influence morphological features, morphology is an integral from the typical phyllome is 2n43 and that from the typical aspect of plant physiology. This is obvious in the titles of caulome is 2n54. The stamen fascicle of Hypericum hooker- many physiological publications such as the following (our ianum is closer to a typical shoot (2n05) than to a typical italics): ‘Influence of magnesium deficiency on rates of leaf phyllome (2n62). The stamens of Arabidopsis have not been expansion, and accumulation, and net analysed in this fashion, but there is good evidence that they assimilation in Phaseolus Šulgaris’ (Fischer and Bremer, are also somewhat intermediate between a typical phyllome 1993); ‘Characterization of calcium\calmodulin—depen- and a typical caulome because in early developmental stages dent kinase homolog from roots showing they exhibit radial symmetry as in caulomes (e.g. Bowman, -regulated ’ (Lu, Hidaka and Feldman, 1994). Thus, morphologically, they are not totally hom- 1996). From these and many other titles it is obvious that ologous to a phyllome such as a . Implicitly or morphology is relevant to physiology. In many other explicitly claiming a total morphological correspondence of physiological publications regardless of whether morpho- all floral appendages is a gross oversimplification. This logical terms are used in the title or not, reference to contrasts strikingly with the precision in the comparison of morphology is made directly or indirectly. Indirect reference DNA, RNA, and protein sequences which is usually may be due to the methodology used. For example, if quantitative (e.g. ‘the flo and lfy genes encode proteins that physiological factors such as hormones are extracted from are 70% identical to each other’ (Coen and Carpenter, leaves or stems, reference to morphological concepts is 1993). A rectification of this discrepancy of precision implied. between the molecular and morphological levels appears highly desirable if we want to achieve a more adequate ReleŠance of non-classical morphological concepts and understanding of plant development. Concretely, with conceptual frameworks regard to stamens, this may imply, for example, that we investigate more precisely the relation between gene action Most of the physiological research that relates to and processes they share with branchlets on one hand and morphology is based on concepts of classical plant mor- phyllomes on the other. In other words to work out the phology such as root, stem, leaf, branch, inflorescence and mosaic of genetic and morphogenetic relations in stamens flower. This tradition is kept alive by research publications and other structures (such as the ) seen as as well as textbooks which usually refer only to classical combinations of processes at different organizational levels morphology. One of the few exceptions to this trend is Taiz ranging from the biophysical molecular to the organismal– and Zeiger’s (1991) Plant physiology. They included a short environmental levels (see also Greyson, 1994). paragraph on the phytomer with a drawing of this morpho- Continuum and process morphology are not only relevant logical unit. However, it is incorrectly delimited because in concrete research situations of genetics and molecular while the phytomer’s axillary (in the axil of its leaf) Sattler and Rutishauser—ReleŠance of Morphology 575 is excluded, the axillary bud of the preceding phytomer is the further question arises as to how these process included. In any case, the reference to the non-classical combinations relate to physiological processes. phytomer concept remains rather inconsequential, since this Process morphology is not only relevant to physiology in concept is not applied in the remainder of the book that many concrete research situations, but also affects the deals exclusively with classical concepts as do almost all general relation of physiology and morphology. Tradition- other books and publications in the field. ally, physiology is said to deal with function, and mor- Although classical morphology is useful and adequate to phology with structure. As pointed out, for example, by a great extent, it is limited (e.g. Rutishauser and Sattler, Woodger (1967), this distinction has led to debates on 1985). Therefore, it is important to complement it with non- whether function determines structure or Šice Šersa. - classical concepts and approaches which present other ger’s process view based on Whitehead’s process philosophy perspectives that may be of interest to plant physiologists (e.g. Birch and Cobb, 1981) and process morphology help to and are obscured by classical morphology. One non-classical overcome such debates and the structure-function (struc- concept is the above mentioned ‘phytomer’, more com- ture-process) antithesis from which they arise. If structure is monly referred to as ‘metamer’ (White, 1984). A metamer seen as process, then it is no longer opposed to function comprises an internode, node, leaf (or leaves, if there is which is also process. From this point of view an organism more than one leaf at the node), the axillary bud(s) of this is seen as process or activity. Morphology deals with the leaf or leaves, and roots, if present. One could see a metamer morphogenetic aspects of this activity, whereas physiology as an assemblage of organs of classical morphology, but one also investigates the activities that accompany morpho- can see it also as an alternative conceptual dismemberment genesis such as metabolism. Since these latter activities are of the whole plant in which the stem-leaf boundary is not integrated with the morphogenetic processes, it is inap- drawn (Rutishauser and Sattler, 1985: Table 1). In this propriate to ask whether the morphogenetic processes latter perspective, the metamer represents the stem-node- determine the physiological ones or Šice Šersa. Both are leaf continuum (Howard, 1974). It may be significant for aspects of an integrated dynamic system. physiological research to take into consideration this stem- Process morphology has further philosophical ramifica- node-leaf continuum, i.e. plant metamerism. Watson and tion with regard to physiology. Traditionally, physiological Casper (1984) reviewed research that supports this con- processes are said to occur within structures such as roots, tinuum from a physiological point of view. They noted that stems, leaves or the whole plant. If, however, structures are metamers may exhibit a degree of autonomy with regard to seen as process, or, more specifically, as process combina- physiological properties such as assimilate or carbon tions, then there is only process or activity. There is no distribution. ‘Thus, metameric units in Phaseolus—consist- longer an agent (or substance) to whom the processes could ing of a section of stem, a trifoliate leaf, and the associated, be ascribed. Thus, we find ourselves in a similar situation as laterally borne reproductive branch—function as internally in physics. As Capra (1983) put it: ‘There is motion but integrated and relatively autonomous physiological units’ there are, ultimately, no moving objects; there is activity but (Watson and Casper, 1984). These units correspond to there are no actors; there are no dancers, there is only the Adam’s (1967) ‘nutritional units’ (Watson and Casper, dance’. 1984). In other plants, other ‘semiautonomous, integrated physiological units’ (IPUs) may occur. ‘Clearly, not all ECOLOGY AND MORPHOLOGY plants are equally subdivided; rather, they exist somewhere on a continuum from total integration to highly localized Ecology deals with the relations between organisms and sectorialization’ (Watson and Casper, 1984). Even if it their environment. In autecology or physiological ecology should turn out that the metameric integration is not the focus is on the interaction of individual organisms and widespread, it is still useful because it complements the environmental factors such as light, temperature, gravity, classical view. Furthermore, it is of heuristic value because etc. (e.g. Billings, 1966: Fig. 2-1). In population ecology the it allows us to ask different questions and pursue research in emphasis is on how populations relate to the environment. a different direction. Population genetics is part of, or closely related to, this The continuum view of plant form has been adopted to an branch of ecology. Community ecology deals with whole even smaller extent in physiology than metamerism. None- communities including the environment. In all of these fields theless, it is relevant. For example, as pointed out by Steeves of ecology, morphology plays a role. This is most obvious in and Sussex (1989), the formation of leaf-like appendages (in autecology or physiological ecology. Many publications Begonia hispida var. cucullifera) without the intervention of report on the interaction of plant structures with the a shoot apex directly on young leaves (Sattler and Maier, environment or analyse the ways in which environmental 1977) is relevant to the question of leaf determination. Since factors affect particular structures. The following are the leaf-like appendages in this Begonia variety form a examples (our italics): ‘Leaf anatomical responses to light continuum with typical trichomes, the question arises of in five tropical Moraceae of different successional status’ how this continuum is based physiologically, i.e. which (Strauss-Debenedetti and Berlyn, 1994); ‘Carbon fixation physiological factors contribute to its manifestation. Ob- profiles do reflect light absorption profiles in leaŠes’ (Evans, viously, such a question cannot be asked unless the 1995). Ecomorphology, which deals with growth forms in continuum between leaves and trichomes is recognized in relation to the environment, continues to contribute to our the first place. If this continuum is seen dynamically, i.e. as understanding of plants within environments (e.g. White, a continuum of morphogenetic process combinations, then 1984; Hagemann, 1989; Marquis, 1996). During the past 576 Sattler and Rutishauser—ReleŠance of Morphology decades, studies of plant architecture have become increas- stem-node-leaf continuum (Howard, 1974). In such a ingly integrated with ecology (e.g. Halle! et al., 1978; Watson continuum the ‘parts’ are no longer separate realities. In a and Casper, 1984; Sachs and Novoplansky, 1995). still more comprehensive view, the whole plant, comprising In population and community ecology the influence of the root and shoot system, can be seen as a continuum. And morphology is less obvious. Also, much work has been finally, this organismal continuum can be understood as carried out without reference to morphology. As White part of a continuous organism-environment system. In this (1984) pointed out, ‘in the huge literature of plant sense, Etherington (1975) referred to the -plant-air- competition, the response [to the environment] is almost continuum (SPAC). From this perspective the plant is no invariably expressed in terms of ’. Here morphology longer distinct from the environment. ‘Plant’ and ‘en- is ignored and thus much detailed information is lost. There vironment’ no longer exist as separate realities. Research are, however, also competition studies that consider mor- conducted from this broader perspective has to integrate phological parameters. For example, Darwinkel (1978) morphology and ecology. How this may be done can be studied tiller demography and the effect of tiller density on illustrated through process morphology and process grain production of winter wheat. Hunter and Aarson thought. (1988), and others have referred to morphology in the As pointed out already, according to process morphology, context of studies on cooperation. structures are seen as process combinations. In two case studies (Sattler and Rutishauser, 1990; Jeune and Sattler, 1992), only morphogenetic processes have been considered. For example, a typical simple leaf was seen as a combination ReleŠance of non-classical morphology of axillant positioning and dorsiventral and determinate White (1979, 1984) pointed out the significance of plant growth. It was pointed out, however, that processes at other metamerism for ecology and other fields. According to organizational levels have to be included for a more this view, metameric plants such as seed plants are built comprehensive analysis (Sattler, 1992). Obviously, the up of segments, called metamers (see Introduction and morphogenetic processes that characterize the leaf are Physiology section). Taking these metamers as the basic combined with processes at the molecular level and processes units of construction (instead of stems and leaves), may of the environment such as solar radiation, cosmic radiation, provide a different perspective. For example, Callaghan gravitation, etc. (e.g. Billings, 1966). In other words, the (1980) analysed productivity and nutrient allocation in dynamics of a leaf are a combination of processes ranging Lycopodium annotinum from this point of view. from local to cosmic dimensions. In this sense, the leaf is Whereas most botanists consider a plant such as a to integrated into a rather universal web of processes. It does be an individual, some authors look upon each module (a not exist just locally as visual perception would have us shoot derived from one apical meristem) as an individual, believe. However, in conducting research we will have to and for others each metamer represents an individual. If confine ourselves to a limited number of processes, which is metamers or modules are identified as individuals, then a one reason why science cannot attain the absolute truth. tree is a population of individual plants. Disregarding Nonetheless, it is important to keep in mind the cosmic somatic mutation, such a population consists of genetically connection. identical individuals. White (1979, 1984) referred to such populations as ‘metapopulations’ in contrast to populations of genetically diverse individuals. The important conclusion EVOLUTIONARY BIOLOGY AND is that once a plant is seen as a sort of population, then MORPHOLOGY principles of population biology apply within a single plant such as a tree. What was previously an individual unit in a Charles Darwin considered morphology the ‘very soul’ of population, is now a population itself. Sachs, Novoplansky natural history which to him was the basis of evolutionary and Cohen (1993) concluded that ‘most plants could be biology. Today, molecular evolution has become a promi- special and interesting intermediates between unitary organ- nent field. Nonetheless, we also want to know how whole isms and clonal populations’. organisms and populations of organisms evolved. Since Continuum morphology also plays a role in ecology. We morphology is an important aspect of whole organisms, it may distinguish the following two aspects of continuum continues to play a major role in evolutionary biology. This morphology: (1) the continuum of non-contiguous parts; is reflected in many publications in this field (e.g. Zimmer- and (2) the continuum of contiguous parts. The continuum mann, 1959; Croizat, 1960, 1962; Meyen, 1973, 1987; of non-contiguous parts has been confirmed using multi- Stevens, 1984; Stidd, 1987; Cronquist, 1988; Hay and variate analysis (Jeune and Sattler, 1992; Sattler and Jeune, Mabberley, 1991, 1994; Takhtajan, 1991; Mabberley and 1992). In this case, parts of different plants such as roots, Hay, 1994). The reader who scans bibliographic sources will stems, leaves and intermediate structures form the con- notice frequent reference to morphological concepts. A few tinuum or, more precisely, the heterogeneous continuum in recent examples of research publications are the following which some areas, namely those of the typical structures, are (our italics): ‘Floral structures and evolution of primitive denser than those of intermediate structures (Sattler, 1996). angiosperms: recent advances’ (Endress, 1994); ‘ in How does this finding relate to ecology? What difference Magnoliidae and the origin of flowers in other subclasses of can it make to ecological analysis? the angiosperms. I. The relationships between flowers of An example of the continuum of contiguous parts is the Magnoliidae and Alismatidae’ (Erbar and Leins, 1994). Sattler and Rutishauser—ReleŠance of Morphology 577 have become expressed in the sites of process combinations ReleŠance of continuum and process morphology characteristic of typical leaves. As noted, this conclusion Evolutionary changes, especially in natural populations, depends on the assumption that the taxa with pinnate leaves are often characterized in terms of changes in gene evolved from ancestors with simple leaves. Even if this frequencies. Although this ‘bean bag’ view offers some assumption should turn out to be incorrect or improbable, insight, it is limited. Evolution is a change in successive the fact remains that the pinnate leaves investigated thus far ontogenies and therefore the study of ontogeny including its combine morphogenetic processes of both simple leaves and morphogenesis is crucial for an understanding of evolution. shoots. Therefore the pinnate leaves remain part of the In classical morphology, structural changes in successive dynamic continuum between shoots and simple leaves ontogenies are usually seen in terms of modifications within (Rutishauser and Sattler, 1997). structural categories. Thus, for example, the evolutionary The extent to which developmental hybridization has modification of roots, stems and leaves have been investi- played a role in evolution must be assessed by future studies. gated. Although this somewhat categorical view has It seems more prevalent than generally acknowledged. One provided insights into evolutionary change, it is limited reason why this evolutionary process has often been because during evolution developmental pathways (or overlooked or ignored is due to the fragmentation under- portions of them) of different structural categories may be lying studies in so-called character phylogeny (Hay and combined (e.g. Lodkina, 1983; Poethig, 1988). Sattler (1988) Mabberley, 1991; Mabberley and Hay, 1994). In these referred to such combination as ‘developmental hybridiza- studies, whole organisms are first conceptually dismembered tion’ because it leads to hybrid structures that combine into parts representing structural categories such as root, features of different structural categories (e.g. Sachs, 1982; stem and leaf. Then parts belonging to the same category Meyen, 1984, 1987; Brugger and Rutishauser, 1989). Instead are compared and it is asked which is derived from which. of ‘hybrid structures’, some plant biologists have referred to For example, is the stamen derived from a phyllome (leaf developmental mosaics (e.g. Rutishauser, 1995) which may homologue)? Such questions preclude that anything else but be only another term for the same concept. In this context, leaf homologues could have been involved. They simplify what is most important to us is the concept not the term matters and misrepresent the basics of evolution. It is well designating the concept. The concept under consideration is known that parts of organisms such as leaves do not evolve non-classical in the sense that hybrid or mosaic structures from each other. Whole organisms and populations of cannot be assigned to structural categories. For example, organisms evolve into each other. In each generation the phylloclades in the Asparagaceae are neither leaf, nor stem, whole organism is reconstructed with or without major nor shoot homologues, but more or less intermediate modifications (e.g. Oyama 1988, 1989; Sattler, 1994: Fig. 7). between these categories because they combine features of Thus leaves or other structures are rebuilt. During this leaf, stem and shoot to varying degrees depending on the reconstruction, processes may be combined in different particular case (see Cooney-Sovetts and Sattler, 1987; for ways and thus novelties may arise (e.g. Sattler, 1988). For other examples of hybrid or mosaic structures see Sattler example, at the sites where leaves arose in the ancestor, and Rutishauser, 1990; Rutishauser and Huber, 1991). processes of both leaves and shoots may be combined. Mosaic or hybrid structures thus form part of the Recent work in developmental genetics has yielded many heterogeneous continuum between typical representatives mutants that illustrate this phenomenon at different levels of structural categories (Sattler and Jeune, 1992). Instead of (e.g. Broadhvest et al., 1992; Sawhney, 1992). There is also perceiving this continuum in static or static\dynamic terms evidence that combination of processes from combinations (Sattler and Jeune, 1992), it can be seen dynamically in characteristic of different structural categories has occurred terms of process morphology (Jeune and Sattler, 1992). during phylogeny (e.g. Sattler, 1988, 1994). To recognize From this point of view, mosaic or hybrid structures are this evidence we have to go beyond the fragmentation of so- process combinations which arose by the combination of called character phylogeny and the categorical framework processes that are normally part of the process combinations of classical morphology. Thus, continuum and process characteristic of structural categories such as leaf and stem. morphology become fundamentally relevant to the way we Developmental hybridization is often ignored because it perceive structural diversity which forms the basis for is thought that it occurs only in very few exceptional taxa hypotheses on evolutionary change. and some artificially induced mutants. Recently, it has been Process morphology is not only relevant to descriptive shown, however, that even common structures such as and reconstructive work on morphological evolution in- pinnate leaves may have been formed through this evol- volving evolutionary processes. It is also relevant to other utionary process (Fisher and Rutishauser, 1990; Sattler and aspects of evolution such as the explanation of evolution in Rutishauser, 1992; Lacroix and Sattler, 1994; Rutishauser, terms of evolutionary theory. A general discussion of 1995; Rutishauser and Sattler, 1997). Pinnate leaves such as evolutionary theory is beyond the scope of this paper. those of Murraya paniculata and other taxa exhibit However, we want to draw attention to one rather significant morphogenetic processes typical of shoots as well as aspect involving the formulation of questions that guide processes characteristic of leaves. If we follow the common research. Traditionally, questions have been asked con- assumption that pinnate taxa in angiosperms evolved from cerning the evolution of structures. From the point of view primitive angiosperms with simple leaves, then we can of process morphology one would rather ask: how have conclude that during the evolution of the pinnate taxa some process combinations changed during evolution? why have morphogenetic processes of shoot process combinations process combinations changed? how and why has the 578 Sattler and Rutishauser—ReleŠance of Morphology dynamic continuum changed? Finally, since the dynamics differing by 1 point will be separated into two different of organisms and the environment are integrated, one categories A and B, whereas students differing by 20 points would ask: how and why has the organism-environment will be in the same category. In plant systematics, distortion system changed? Since dynamics are more adequately due to the use of two-state or multi-state characters is also represented by verbs than by nouns, a linguistic challenge is a problem. Unfortunately, there are additional distortions to develop a verb-based language that avoids nouns (Sattler, that are revealed by continuum morphology. These distor- 1993). tions are due to the categorical framework of classical plant morphology. According to that framework, every structure has to be classified (homologized) into mutually exclusive SYSTEMATICS AND MORPHOLOGY structural categories. Since there is a continuum between Systematics has been defined as ‘the scientific study of the these categories (Jeune and Sattler, 1992; Sattler and Jeune, kinds and diversity of organisms and of any and all 1992), structures intermediate between typical representa- relationships among them’ (Simpson, 1961). ‘Relationship’ tives of the categories must be forced into one or the other may be expressed in terms of similarity (as in numerical category. Thus, natural relationships are distorted. It should ) or presumed phylogenetic connection (as in be noted that this problem is the same in both phenetic and phylogenetic taxonomy or cladistics). Regardless of how phylogenetic systematics. The challenge for both is to ‘relationship’ is seen, the basis for its evaluation is usually surmount this problem through continuum morphology. a list of characters and character states. Traditionally, these There may be cases in which distortions influence the characters have been mainly morphological, for example, classification system to only a minor extent or not at all. various morphological aspects of flowers, leaves and other This would have to be shown, however, through detailed structures. Today, molecular characters are often used. analyses. In other instances, distortions may compound to Nonetheless, morphological characters continue to play a such an extent that classification systems are greatly affected fundamental role. When molecular data are used, they by them (Rutishauser, 1997). In extreme cases this is supplement morphological characters, or the systems de- intuitively obvious without rigorous analyses. For example, rived from molecular data are tested against those based on in the genus Utricularia (bladderworts) there are species morphological characters. It is interesting to know to what such as U. foliosa whose morphology deviates so much from extent molecular systems are correlated with morphological the typical root-stem-leaf organization that there is ‘no ones. Since whole organisms and their structures contain clear distinction between roots, stems and leaves’ (Mab- more information than an assemblage of molecules including berley, 1987). If, in a systematic comparison with taxa of a genes, relationships based on morphological characters more conventional morphology, we draw up a list of root, supersede those founded on molecular data. This is due to stem and leaf characters, distortion seems unavoidable. emergence, a phenomenon that can be observed even at the Arbitrary decisions would have to be made concerning the inorganic level. For example, water has emergent properties classification (homologization) of parts. For example, what that are absent in hydrogen and oxygen, its component according to one author is a leaf, to another one is a parts. Similarly, any plant structure has emergent properties (branch), or even part of a root-system (see Brugger and that cannot be observed in the constituent molecules. Rutishauser, 1989; Sattler and Rutishauser, 1990). Different Therefore, a classification system based on morphological phenetic or phylogenetic relationships would result depend- characters reflects information that is lacking in a system ing on which homologization is accepted. founded on molecular data (e.g. Sattler, 1986). There is a further problem that affects not only the In any case, a cursory look at modern classification comparison of Utricularia species, but also taxa of more systems, both phenetic and phylogenetic, will easily convince conventional morphology. Plants can be conceptually us that morphology plays a major role in systematics (e.g. dismembered in different ways (Rutishauser and Sattler, Cronquist, 1988; Takhtajan, 1991; Woodland, 1996). 1985: Table 1). Besides the classical root-stem-leaf concep- Although molecular data will be increasingly used, mor- tualization, there are several others, one of them the phology cannot be abandoned if we want to retain maximum metameric model according to which the plant shoot consists information. of metamers only. If the metameric or other models are used to score characters, a rather different list of characters may result. How would this affect classification? We may indeed ReleŠance of continuum and process morphology obtain different classifications even for rather conventional Although many quantitative characters are used in taxa if we used different conceptual dismemberments of the modern systematics, two-state characters are also commonly plants. This would have to be demonstrated, however, by employed. An example of a two-state character is: flowers rigorous analyses. In extreme cases such as Utricularia it is large (state 1) or small (state 2). Stevens (1991, 1996) has probable that different homologizations would have an drawn attention to possible pitfalls of two-state and even impact on classification. Thus we would have to accept a multi-state characters. Whenever we deal with a continuum, number of different classifications or arbitrarily select one of dividing it into states is arbitrary and may lead to distortions them. Process morphology, however, presents another as in the grading schemes employed at most universities: if alternative. Instead of arbitrarily assigning plant parts to the grade B ranges from 65–79, and A from 80–100, a mutually exclusive categories such as stem or leaf, structures, student with a mark of 79 will receive a B, whereas students or even whole plants, could be seen as process combinations with grades of 80 to 100 will obtain an A. Thus two students and these process combinations could form the basis for the Sattler and Rutishauser—ReleŠance of Morphology 579 construction of phenetic or phylogenetic classification example, an ecologist may restrict him\herself to biomass systems (see also Hay and Mabberley, 1994). analysis which ignores morphology. But such analysis, Continuum and process morphology have still broader although useful, provides only a very limited understanding. implications for systematics. Usually the aim of systematics Reference to morphological concepts such as leaves, is to construct classification systems in which groups of metamers or morphogenetic processes will greatly enlarge organisms (taxa) are related hierarchically. In continuum the scope and depth of ecological understanding (e.g. White, and process morphology neither mutually exclusive group- 1979, 1984). ings nor hierarchical structures are present. The notion of a In recent decades, morphology has undergone funda- continuum defies both. Relationships, however, can be mental conceptual, theoretical and philosophical changes established between any points in the continuum. Com- (see Introduction). These changes lead to different questions patible with this view, phenetic continua of organisms or and may redirect the course of research in morphology and taxa could be constructed so that the emphasis would be other fields to which it is relevant. Therefore, a knowledge again on relationship instead of a hierarchy of mutually of recent fundamental innovations in morphology is exclusive groups. Since any organism or group of organisms important for progress in other fields. In this paper we have can be related to many others, this approach leads to a drawn special attention to the idea of a dynamic continuum relational or, more precisely, a multi-relational view which and we have underlined the manifold implications and contrasts with the categorical and hierarchical view of consequences of this idea for plant research. We do not nature. As many relationships are established, a network of claim that traditional morphology has been devoid of relations results. Hence, the underlying structure is a net dynamic and continuum thinking. It has, however, been rather than a hierarchy. It seems that in many ways nets or constrained by the assumption of a more or less rigid networks are more adequate representations of nature than categorical framework. Continuum and process morpho- hierarchies, although the latter may have a limited usefulness logy transcend this constraint to a great extent and therefore (Sattler, 1986). allow questions and answers beyond the scope of traditional The phylogenetic systematist may argue, of course, that classical morphology whose concepts and theories are often phylogenetic systems are that correspond to hier- taken for granted by researchers in non-morphological archies. We know, however, that at the species (or even disciplines such as molecular genetics, ecology and evol- genus) level reticulate evolution may occur (e.g. Rieseberg, utionary biology. 1991). At higher ranks, reticulation due to horizontal gene Morphology is also relevant to ways of thinking in plant transfer has been documented (e.g. Syvanen, 1994). There- biology and biology in general. Since ways of thinking in fore, even in phylogenetic systems nets may be a more biology affect the human condition and society, morphology adequate representation of natural relationships and hier- contributes directly or indirectly to human and planetary archies may be seen as somewhat simplified reconstructions. welfare (e.g. Rutishauser and Sattler, 1985; Sattler, 1986, Future research will have to clarify to what extent nets and 1993; Kirchoff, 1995). hierarchies are appropriate. In the meantime, it may be wise to keep both schemes in mind. They may indeed complement ACKNOWLEDGEMENTS each other (on the notion of complementarity see Ruti- shauser and Sattler, 1985, 1987, 1989; Sattler, 1986). This research was supported by grant A2594 from the Natural Sciences and Engineering Research Council of Canada (NSERC) to the first author. We thank Alexander CONCLUSIONS Bernhard and Rajinder Dhindsa for critical comments on It is often assumed that progress in plant morphology has the first draft of this manuscript and Joanne Smith for (almost) come to an end and that, as a consequence, typing all versions. morphology is only of peripheral importance or none at all. This attitude manifests itself, for example, in the fact that at LITERATURE CITED many universities, plant morphology is no longer taught or Adams MW. 1967. Basis of yield component compensation in crop has been relegated to a peripheral position. As a result, most plants with special reference to the field bean, Phaseolus Šulgaris. students of plant biology—and professors as well—are Crop Science 7: 505–510. generally ignorant about morphology. From their point of Arber A. 1946. Goethe’s botany. 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