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Capitula in the Asteridae: A Widespread and Varied Phenomenon.

I. Abstract

The presence of capitula, the head-type of inflorescences, is widespread in the Asterideae. Several families, predominantly terminal in the clade, display the tendency of maximizing reproductive output by condensing indeterminate inflorescences to the point of capitulum formation. This is accomplished by the process of halting or suppressing development of the internodes, an example of paedomorphosis of the progenesis type. This tendency is either infrequent or absent in the basal members of the Asteridae. When inflorescence condensation is present, closely related taxa often demonstrate the progression of the paedomorphosis. More examples of capitulum formation are found in the more advanced families, culminating with the Asteraceae, almost all of which display fully condensed capitula of some sort. Other phenomena are also apparent besides the basic inflorescence condensation. Edge effects are often seen, ranging from a mere crowding of the outermost flowers to the formation of additional flower types. In some taxa, inflorescence condensation continues beyond the basic capitulum form, yielding even more condensed inflorescences that then become determinate. More highly condensed inflorescences have independently evolved several times in the Asteraceae, and some tertiarily condensed inflorescences have evolved as well.

Zusammenfassung

Die Anwesenheit der Capitula oder der Kopftypen ist bei den Asterideae weit verbreitet. Mehrere Familien, besonders die in den Cladus endenden, zeigen die Tendenz zur Hochstproduktion indem sie unbestimmbare Infloreszenz bis zu dem Zeitpunkt der Capitulumbildung produzieren. Dies kommt durch einen besonderen Prozess zustande, in dem die Architektur der Blutenentwicklung verzogert oder unterdruckt wird--ein Beispiel von Paedomorphose des Progenese Typs. Diese Tendenz erscheint anfanglich bei den Grundgruppen der Asteridae nur selten oder garnicht.

Wenn Infloreszenzkondensation in Erscheinung tritt, so demonstrieren die nahe verwandten Taxa oft die Entwicklung von Paedomorphose. In den mehr fortgeschrittenen Familien finden sich noch weitere Beispiele von Capitulumformation, die dann in den Asterideae gipfeln. Fast alle von ihnen zeigen voll kondensierte Capitula verschiedener Art. Neben der grundlegenden Infloreszenzkondensation sind auch noch andere Phanomene zu beobachten. Es zeigt sich oft, dass Randeffekte verschiedenartige Resultate haben--vom lediglichen Anhaufen der aussensituierten Bluten bis zur Bildung von weiteren Blutentypen. In einigen Taxa wird die infloreszente Kondensation uber die Grundform des Capitulum hinaus witergefuhrt. Dadurch vermehren sich die kondensierten Infloreszenzen, die schliesslich definitiv werden. Sekundarerweise haben sich kondensierte Infloreszenzen mehrere Male unabhangig zu Asteraceae entwickelt, und ausserdem existieren auch einige tertiare Infloreszenzen.

II. Introduction

The indeterminate inflorescence known as a "capitulum" (sometimes "head") is most often invoked as one of the defining characteristics of the very highly evolved family, the Asteraceae (Harris & Harris, 1994; Jeffrey, 1978). In an introductory vascular plant morphology or taxonomy class, the indeterminate Asteraceaous head is usually presented as the only example of the capitulum inflorescence type (Gifford & Foster, 1988; Walters & Keil, 1977). In reality, this type of inflorescence is found, with various minor modifications, in several other families in the Asteridae and elsewhere, including even the Monocotyledonae. Most of the non-Asteraceae families with capitula are also closely related to the Asteraceae, making the presence of capitula an interesting synapomorphy between these highly evolved members of the A steridae.

A capitulum is usually defined as an indeterminate inflorescence that matures in an acropetal, centripetal, or racemose (Cronquist, 1977) fashion where all of the flowers or florets are sessile and are attached to a receptacle that may be wide and flattened, elongated, convex, concave, or somewhere in between. Involucral bracts are often present and effectively perform the function of sepals by protecting the young capitulum as it develops. Some capitula, however, mature in a basipetal or centrifugal pattern (Cronquist, 1977; Payer, 1857) and are then logically termed "determinate inflorescences" (Classen-Bockhoff et al., 1989; Harris, 1994). Examples of such inflorescences may be found throughout the Asteraceae and are an apparent opposite of the indeterminate norm (see Fig. 1). How does this come about? In a few even more extreme examples, some condensed heads mature neither acropetally nor basipetally and thus seem to have no discernable pattern of maturation at all. Is development truly chaotic in such i nflorescences? Or is some pattern present that is on too fine a scale to be easily noted?

It is clear that the definition of "capitulum" must be expanded and clarified to include such inflorescences without obscuring information.

A. MATERIALS AND METHODS

Living material was collected from various sources: natural populations in situ, grown from seed, and from the collections of several botanical gardens (Table I). Several individual plants of each species were sampled from each population, and in some cases more than one population was sampled.

Inflorescences of all stages were fixed in formalin-acetic acid-alcohol (FAA): 90 cc 50% ethanol: 5 cc 37% formalin: 5 cc glacial acetic acid. Voucher specimens were collected and are deposited in various herbaria (see Table I). The preserved material was dissected and examined in 95% ethanol. Often, some of the flowers or other structures were removed to facilitate examination of the remaining structures. Specimens were then dehydrated in an alcohol/acetone series and critical-point dried in a Denton DCP-1 or a Samdri PVT critical point dryer. They were then were mounted on SEM stubs and coated with gold-palladium in a Hummer II sputter-coater. The prepared floral material was studied with a Hitachi S-500 SEM at 20 to 25 kV (Botany Department at Louisiana State University) or a Cambridge Stereoscan 250 Mk2 SEM at 10 kV (Botany Department at the National Museum of Natural History, Smithsonian Institution). Representative micrographs were taken of the various ontogenetic stages.

B. TYPES OF CAPITULA

Numerous variations on the capitulum exist in nature, despite the simplistic definitions of capitula generally found in texts. Capitula are amply represented in the Asteridae and can also be found in every other subclass of the Magnoliopsida (see Table II) and even in a few of the Liliopsida. It is obvious that condensation of an elongated indeterminate inflorescence to a capitulum has occurred independently numerous times in the evolution of the Asteridae and other taxa, an example of widespread convergent evolution.

The capitulum type of inflorescence that is normally associated with the Asteraceae is the most common form of this type of inflorescence. The morphology of such a capitulum may have altered over evolutionary time, resulting in a secondary inflorescence or syncephalium (Harris, 1994; Weberling, 1989). This is accomplished by the failure of the inflorescence pedicels to elongate late in development, yielding at anthesis a more or less loose conglomeration (depending on the taxon) of primary heads. This condition is fairly common and may be noted in various degrees of conglomeration in the genera Nassauvia (Mutisieae), Echinops (Cardueae), Elephantopus (Vernonieae), and Espeletia (Heliantheae), to name but a few. Under certain circumstances, this type of inflorescence condensation may occur again, as in Lagascea (Heliantheae) (Harris, 1994; Kunze, 1969), thus yielding a tertiarily condensed syncephalium. Unequivocal examples of tertiary syncephalia are rare in the Asteraceae (found only in four genera to date) but are often found in other families such as the Dipsacaceae and Calycer aceae. Although conjectured (Petit, 1988), no definite example of quaternary inflorescence condensation has been documented in the Asteraceae or any other family.

1. Primary Capitula

Primary capitula are the most basic type of the head inflorescences. As used here, these are capitula that initiate flowers and undergo development and anthesis in a more or less strict acropetal or centripetal pattern.

Despite the apparent simplicity of the primary capitulum as defined above, a great deal of morphological variation exists, almost all of which is exemplified by taxa in the Asteraceae (Leins & Erbar, 1987). It is thus most efficacious to review the established Asteraceae terminology for primary capitulum morphology:

* Capitulum: A condensed type of indeterminate inflorescence in which all of the flowers are sessile and are located on a receptacle and are subtended involucral bracts (phyllaries). Also known as "head," "cephalodium," and "calathidium" (Weberling, 1989).

* Disciform: A capitulum with at least two types of tubular disk flowers (for example: hermaphroditic and female) but lacking ray flowers (Bremer, 1994).

* Discoid: A capitulum with only one disk flower type, also lacking ray flowers (Bremer, 1994; Leppik, 1977).

* Radiate: A capitulum possessing ray flowers around the periphery of the capitulum. These ray flowers are zygomorphic and often showy but may also be small and relatively inconspicuous (Bremer, 1994; Leppik, 1977).

* Homogamous: A capitulum with flowers that all have the same sexual form, usually hermaphroditic (Bremer, 1994).

* Heterogamous: A capitulum with flowers that have more than one sexual form (Bremer, 1994).

* Synflorescence: All of the individual inflorescences considered together; for example a corymbose synflorescence is often found in the genus Solidago. Also known as "incapitulescence" (Petit, 1988; Walters & Kiel, 1977) and "conflorescence" (Leppik, 1977).

2. Higher-Order Condensations

In some taxa, further evolution of the inflorescence form has taken place to yield a more complex inflorescence termed a "syncephalium" (Harris, 1994; Kunze, 1969; Weberling, 1989), a "synfloreszenz" (Goebel, 1931) or "pseudocephalium" (Troll, 1928). Syncephalia in the Asteraceae have long been the subject of scrutiny and conjecture (Schultz-Bipontinus, 1861, 1863). As Schultz-Bipontinus noticed in his survey of taxa of the Asteraceae, a very common (but by no means the only) manifestation of higher-order inflorescence condensation is the reduction of the primary capitulum to a one-flowered state (Fig. 1b, upper pathway). Despite the reduction in flower number, primary capitula in such a syncephalium retain their individual involucral bracts, an indication of their true nature. Indeed, it was the presence of this extra "chaff" on the surface of the inflorescence receptacle that originally heralded the notion that something about the morphology of these inflorescences was unusual.

C. ONTOGENY OF THE CAPITULUM

1. Primary

The formation of the primary Asteraceae capitulum has been extensively studied by researchers in agriculture and horticulture who have an interest in describing the histological events and quantifying the environmental requirements in a few economically important taxa of the Asteraceae (see the exhaustive reviews in Halevy, 1985, 1986). Chrysanthemum morifolium, in particular, has been much studied (Cathey & Borthwick, 1957; Charles-Edwards et al., 1979; Horridge & Cockshull, 1979; Horridge et al., 1985; Popham, 1964; Popham & Chan, 1950, 1952).

Other workers have found various species of the Asteraceae ideal for studies of plant photoperiodism, which then also yield data regarding the ontogeny of the capitulum. Aspects of the physiology, development, and flowering of the cocklebur, Xanthium strumarium, have been extensively investigated (Maksymowych, 1990). Xanthium was one of the first short-day plants documented (Naylor, 1941; Salisbury, 1985, 1990, and references therein) and is still popular as a subject for day-length (and other) studies.

Reproductive or inflorescence meristems differ in several aspects from vegetative apical meristems. Functionally, the inflorescence apex becomes determinate (Steeves & Sussex, 1989) and irreversible (Schwabe, 1959). In the Asteraceae, in particular, the structural differences between the inflorescence and the vegetative meristems are marked (Horridge & Cockshull, 1979; Popham & Chan, 1952). The vegetative apex is relatively small, highly domed, and densely meristematic (Rauh & Reznik, 1953). As the apex switches over to the reproductive phase in response to the appropriate environmental cues, it increases in size, and the overall shape is altered as the apex gradually broadens and flattens (Popham & Chan, 1950, 1952). Figures 2 and 3 demonstrate the beginning of the inflorescence meristem ontogeny for two homogamous capitula (one in the Asteraceae, and one in the Apiaceae). Figure 4 demonstrates the same for a heterogamous capitulum. Cells in the interior of the meristem become highly vacuolate, eventually l eaving only a mantle of meristematic cells at the surface. Rauh and Reznik (1953) documented the various degrees of meristematic activity of the histogenetic zones in the developing inflorescences of representative species of Asteraceae, as well as some species of Dipsacaceae and Campanulaceae. Differential activity by the Markmutterzellgruppe (central mother-cell zone) was found to produce the different forms of the capitula, from the flat or even slightly concave receptacles to the extremely convex or conic forms.

Often, a distinct intermediate stage is produced after the vegetative apex begins to enlarge by broadening and flattening but before the inflorescence meristem is recognizable as such (Molder & Owens, 1973, 1985). This "transition apex" is distinguished from the vegetative apex by its larger size and broader shape but lacks apical derivatives such as involucral bract primordia, floral primordia, or receptacular bract primordia (Popham, 1964; Popham & Chan, 1952). In Chrysanthemum morifolium, such a meristem was termed a "crown bud" and was artificially produced under certain light regimens. It failed to ever initiate flower primordia or, indeed, primordia of any type. Similar results were found in studies of Cosmos bipinnatus (Molder & Owens, 1973, 1985). Cathey and Borthwick (1957) found that the reversibility to a vegetative state and the reinduction of the inflorescence meristem from the crown-bud stage were dependent upon successive exposures of red and far-red light, respectively. Similarly, Salisbury ( 1985, 1990) found that the inflorescence meristem prior to floral initiation (i.e., the transition meristem) of Xanthium strumarium can also be forced to revert to the vegetative state.

When present, the transition apex is similar to the inflorescence apex in size and shape, but the ongoing cell division contributes solely to a gradual increase in size. Some species of Asteraceae can remain in this stage indefinitely (Harris, unpubl.; Pophan & Chan, 1952), presumably awaiting the right environmental cue(s) to trigger the flowering phase.

Other species, such as Chrysanthemum segetum, pass through the expansion stages rapidly without pausing at a recognizable transition phase (Nougarede, 1986; Nougarede et al., 1987). The manner in which the vegetative apex (indeterminate) is transformed to reproductive (determinate) in the Asteraceae was demonstrated as being similar to the transformation that vegetative apices undergo as they convert into individual floral meristems (Wetmore et al., 1959)--another example of the analogy of single flowers to the capitulum type of inforescence (Burtt, 1977).

Regardless of how it occurs, eventually the reproductive meristem is irrevocably committed to flowering. For instance, initiation of involucral bract primordia was found to herald the irreversibility of the Chrysanthemum morifolium inflorescence meristem (Horridge & Cockshull, 1979).

Ongoing inflorescence ontogeny, following the commitment stage, has also been studied extensively. Cathey and Borthwick (1957) found that red light inhibits flower initiation and that far-red light "repromotes" flower initiation in Chrysanthemum. They later (1964) sampled C. morifolium apices at regular intervals after exposing the plants to varying amounts of inductive photoperiods. In this way, they were able to delimit the duration (in days) of each developmental stage of this timetable. Similarly, Marc and Palmer (1978) were able to determine absolute time values for inflorescence initiatory events: six or seven flower primordia per day were initiated on the meristematic surface of the inflorescence of the Helianthus cultivars they utilized.

However triggered, floral initiation on the meristem of the primary capitulum proceeds in a more or less acropetal or centripetal fashion. In species with homogamous capitula, acropetal initiation is the norm (Battjes, 1994; Harris, 1995: tab. 3). Floral initiation proceeds in spiral parastichies until most or all of the uncommitted inflorescence meristem is used up. This is amply demonstrated by numerous Asteraceae species such as Palafoxia calosa (Heliantheae) (Fig. 2), as well as taxa in other families such as Eryngium carlinae (Apiaceae) (Fig. 3).

Acropetal initiation is not as clear-cut a phenomenon in heterogamous or radiate capitula. Numerous examples of a lag in the initiation and subsequent development of the ray or peripheral flowers are found in the Asteraceae (Gottlieb & Ford, 1987; Harris, 1995: tab. 4; Horridge et al., 1985; Molder & Owens, 1973, 1985) and can be seen in Bidens pilosa (Fig.4). At times, the lag in peripheral flower initiation and development is so pronounced as to produce a bidirectional pattern with regard to the ray flowers (basipetal) and the disk flowers (acropetal) (Harris et al., 1991), as seen in Erigeron philadelphicus L. Both types of flower primordia are initiated in spiral parastichies that stem from the "equator of origin," located approximately midway between the base and apex of the inflorescence meristem. In such cases, initiation proceeds in both directions until all uncommitted portions of the inflorescence meristem are filled with flower primordia.

It must be stressed that these deviations from the strictly acropetal pattern of events occur only when more than one type of flower is present on the primary capitulum. The initiation and ontogeny of the two flower types have diverged (as a result of different functional selection pressures), yielding such seemingly confusing events in t e heterogamous or radiate head.

2. Secondary

Various aspects of the ontogeny of secondary capitula have also been investigated in several Asteraceae taxa that display secondarily condensed capitula. The occurrence of secondarily condensed heads is fairly widespread in the Asteraceae, as evidenced by the numerous studies of secondary capitulum ontogeny or bauplans (Classen-Bockhoff, 1992, 1996; Kunze, 1969; Leins & Gemmeke, 1979; Petit, 1988; Rauh & Reznik, 1953; Wagenitz, 1976; Weberling, 1989). Not as immediately obvious in the literature, but as telling, are the reports that secondary aggregations of heads are present in particular taxa (Bremer, 1994; Heywood et al., 1977). A review of the literature concurrent with an examination of representative taxa available in herbaria has brought to light approximately 65 genera with this character, some monotypic and some quite large, distributed among nine tribes, in all three subfamilies of the Asteraceae (Table V). This is a conservative estimate, and as other taxa become available for study, the numbers w ill no doubt be revised upward. Of the 65 genera documented thus far with secondary heads, 39 are monotypic. Other genera are moderate- to large-sized, such as Echinops (120 spp., and thus the largest asteraceous genus to display secondary capitula), Sphaeranthus (40 spp.), and Elephantopus (30 spp.). (Since the phenomenon of secondary condensation is well-documented, it will not be demonstrated with figures herein.)

In some instances, all species in a genus display secondary condensation, as in the large genus of Echinops or the monotypic Quinqueremulus (Bremer, 1994). In some genera only a single species displays secondary heads in a genus with otherwise uncondensed heads, as in Dyssodia decipiens (Bartl.) M. C. Johnston (Classen-Bockhoff, 1992). Between these two extreme situations stand other genera, such as Nassauvia Comm. ex Juss., with 39 species, at least 13 of which can be considered truly condensed into secondary heads. Other species of Nassauvia possess inflorescences that are clearly intermediate stages along this evolutionary pathway of primary capitulum aggregation (Harris, unpubl.).

As far as secondary inflorescences are concerned, most often and most thoroughly studied is the large, Old World genus Echinops (Kunze, 1969; Leins & Gemmeke, 1979; Petit, 1988; Rauh & Reznik, 1953; Wagenitz, 1976). Other taxa displaying secondarily condensed capitula, such as Dyssodia decipiens (Classen-Bockhoff, 1992), have also been investigated, but Echinops reigns supreme in the literature. Although Echinops has one-flowered primary capitula (Petit, 1988; Schultz-Bipontinus, 1861) other taxa, such as Dyssodia decipiens, display primary capitula with more than one flower (Classen-Bockhoff, 1992; Weberling, 1988). Development will be described in Echinops, which is typical of ontogeny for a secondarily condensed capitulum.

The initiation, ontogeny, and subsequent anthesis of the secondary capitulum is homologous to that of a synflorescence or collection of primary capitula (Classen-Bockhoff, 1992; Harris, 1994; Kunze, 1969; Rauh & Reznik, 1953); that is, the individual or primary capitula are initiated in an acropetal sequence and develop acropetally, but they then undergo anthesis basipetally. The vegetative meristem of Echinops is small and relatively flat, with a tunica composed of two layers (Raub & Reznik, 1953). As the inflorescence meristem differentiates from the vegetative apex, the tunica becomes three layers thick, and the meristem enlarges and becomes first hemispherical and then conical. The primary capitula (one-flowered heads in Echinaps) are initiated in a spiral, acropetal sequence on the large inflorescence meristem (Leins & Gemmeke, 1979; Rauh & Reznik, 1953). This sequence of acropetal initiation is the same for the initiation of individual primary inflorescences in a synflorescence, nicely seen in the SEM photomicrographs of Lactuca sativa L. by Moncur (1981). In either case, care must be taken in differentiating between the primary capitulum meristems and the apical synflorescence meristem that produces the former, as they are often similar in size and appearance.

In rapid sequence (Rauh & Reznik, 1953), all of the primary capitula of Echinops (whether one-flowered or not) become equalized in size regardless of their position. Immediately following this stage, the primary capitula begin to differentiate in a basipetal sequence (Classen-Bockhoff, 1992). In Echinops, the first sign of this basipetal differentiation is the production of involucral bracts subtending each single-flowered primary capitulum (Leins & Gemmeke, 1979). For Lactuca, the same sequence is followed: the terminal primary capitulum differentiates first, followed in basipetal succession by the remaining primary capitula in the synflorescence (Moncur, 1981). Further differentiation, such as the initiation, early ontogeny, and maturation of flowers, continues in this basipetal fashion. Indeed, even anthesis proceeds basipetally.

3. Tertiary

Tertiarily condensed capitula are much rarer than secondarily condensed heads. In the Asteraceae, only four genera have been identified as such to date: Gundelia (Classen-Bockhoff et al., 1989), Lagascea (Harris, 1994; Kunze, 1969), Platycarpha, and Paralychnophora (Harris, unpubl.) (Table III). Tertiary capitula are also found in the Calyceraceae (current study), a small South American family closely allied to the Asteraceae, if not the actual sister-taxon to the Asteraceae (Bremer, 1994; Hansen, 1992). Tertiary capitula are also reported in the Goodeniaceae (Carolin, 1978) and the Brunoniaceae (Carolin, 1978; Erbar & Leins, 1988), two other families that are very closely related to the Asteraceae (Bremer, 1994). Preliminary investigations suggest that tertiary capitula are also present in Adoxa moschatellina L. (Adoxaceae) (Harris, unpubl.). In contrast to the varied or less canalized pathways of secondary capitula ontogeny, tertiary capitula all exhibit a reduction of the primary capitula to a one-flowere d state. Presumably, this reduction results in an evolutionarily more malleable subunit of a secondary capitulum that may be further condensed into the tertiary state (Fig. 1c).

As described for Gundelia tournafortii L. (Classen-Bockhoff et al., 1989) and the six species of Lagascea (Harris, 1994) represented by L. helianthifolia, the main events occurring during the ontogeny of tertiary capitula are circumscribed; this holds true for the species of Asteraceae cited above as well as for Calycera leucanthema (Fig. 5) and C. herbacea (Fig. 6) in the Calyceraceae. Differences between taxa do, of course, exist and include the following: number and morphology of associated bracts, vestiture, absolute size of the syncephalium at anthesis, number of individual flowers and secondary capitula, and degree of fusion between the neighboring structures. There are enough dissimilarities between the taxa to lend credence to the assertion that these manifestations of tertiary capitulum condensation occurred independently during the evolution of the Asteridae. The more canalized pathway of syncephalium ontogeny noted in the six species of Lagascea (Harris, 1994) indicates that tertiary condensation occurred only once, early in the evolution of that lineage.

The syncephalium meristem differentiates from the vegetative meristem by enlarging and becoming flatter and broader (Fig. 5.2). The syncephalium subunit primordia (SSPs) are initiated acropetally in orderly parastichies on the capitulum. These SSPs are homologous to secondary capitula. The SSPs enlarge and differentiate in the acropetal sequence set by their initiation. Within an individual SSP, differentiation will proceed basipetally, as described for the secondary capitula above (Fig. 5.4). This is demonstrated as the SSP subdivides and first yields a recognizable meristem in the central or terminal position. This meristem will soon differentiate into a one-flowered primary capitulum, complete with involucral bracts. Somewhat later, one or more meristems differentiate from the uncommitted meristem of the SSP surrounding the base of the terminal primary capitulum (Fig. 5.5). These meristems will also produce one-flowered primary capitula surrounding the terminal capitulum. The lag in timing demonstrated by these subsequently produced capitula is maintained during later stages of development in stage and size as compared with the terminal capitulum in an SSP (Figs. 5.5 & 5.6). This pattern is often evident at anthesis (Figs. 6.1 & 6.4), although it is difficult to ascertain. The complexity of this pattern has often seemed, to the casual observer, to be a random order of anthesis.

The sequence of initiation, floral development, and anthesis is thus different for each type of capitulum, and in each case it echoes events that take place very early in the ontogeny of the inflorescence. A summary of these differences is given in Table IV, using some of the terminology introduced above.

D. EVOLUTION OF THE CAPITULUM

As demonstrated by the widespread occurrence of capitula in the Magnoliopsida and the Liliopsida, capitula have evolved independently many times, The term "primary "is used here to indicate the ancestral or primary condensation event that produced the capitulum from some sort of elongated indeterminate inflorescence (Fig. la) (Burtt, 1977; Harris, 1994; Schultz-Bipontinus, 1861, 1863; Weberling, 1989) or from a racemose umbel (Small, 1918; Stebbins, 1974). Undoubtedly, the capitula found in the various taxa of the Magnoliidae (Table V) arose from different progenitors.

An alternate view to an indeterminate inflorescence as a precursor for the typical asteraceous capitulum was suggested by Cronquist (1977), who proposed that the ancestors to the Asteraceae had a cymose (determinate) inflorescence that was condensed into a head, which then "was gradually converted" from the cymose or determinate state to the racemose or indeterminate state. Cronquist based this alternative theory on the inflorescence review paper by Rickett (1944). However, a close examination of Rickett's paper does not substantiate the view attributed to him by Cronquist. For those taxa such as Dipsacus (Dipsacaceae), the primary capitulum may have evolved from an elongate determinate inflorescence yielding an unusual anthesis pattern: bidirectional from a midline (Jurica, 1921). Other taxa in the Dipsacaceae (Knautia, Scabiosa) display tertiarily condensed heads, as described above.

A condensation event from an indeterminate ancestor, as illustrated in Figure la, easily can have occurred with relatively few alterations in ontogeny. Figure 7 illustrates the young inforescence of Lobelia tupa. This taxon commonly produces racemes of great height (to 3 m or more). The early stages of inflorescence development, however, display a compact shape remarkably similar to that of a capitulum (compare with Fig. 2, Palafoxia calosa). Elongation of the raceme takes place late in ontogeny, long after the flowers are formed by the inflorescence apex. If elongation failed to occur, a primary capitulum would be born. Such a spontaneous mutation could be simply inherited involving a single or very few genes. The widespread distribution of primary capitula in the Magnoliidae (Table V) lends indirect evidence for this.

A similar sequence of events is hypothesized to produce the higher-order capitula, once the primary capitulum has evolved and become canalized in a taxon. For example, the early stages of development of the entire synflorescence of Lactuca sativa (Moncur, 1981) demonstrate the similarity between a collection of primary capitula prior to elongation and a secondary capitulum such as that found in Dyssodia decipiens (Classen-Bockhoff, 1992).

Ill. Distribution of Capitula

Many instances of capitula (primary or otherwise) occur in the Magnoliopsida (Cronquist, 1981; Philipson, 1947, 1953). The distribution of families that have taxa displaying capitula is extremely broad (see Table V; Cronquist, 1981; Philipson, 1953). Capitula appear in every subclass of the Magnoliopsida. Some Liliopsida taxa, such as the Eriocaulaceae, also display a head type of inflorescence (Cronquist, 1981). Those that share the greatest similarities are found in the Asteridac. The Asteridae as presently delimited are a large taxon with many highly evolved members (Chase et al., 1993; Downie & Palmer, 1992). It is likely that the morphological similarities of the capitula of Asteridae stem from similar sorts of evolutionary pathways undertaken independently (convergent evolution). If one looks further afield, other capitula may be found that are more and more dissimilar to those found in the Asteraceae; for example, the primary capitula of the Proteaceae (Burtt, 1977).

IV. Summary

The capitulum type of inflorescence has a wide distribution in the Asteridae and can also be found in all other subclasses of the Magnoliopsida (sensu Cronquist). Given the distribution, it is clear that capitula have evolved independently many times.

The primary capitulum is characterized by an indeterminate or acropetal sequence of floral initiation, development, and anthesis. Deviations from the acropetal modus operandi occur when peripherally located flowers differ in morphology from those that are more centrally located. The peripheral flowers tend to lag behind in initiation and/or development, occasionally evident even in anthesis. The evolution of such an inflorescence was most probably from an indeterminate elongate inflorescence, such as a raceme or a spike.

Secondarily condensed heads are also fairly common. Expression of secondary heads is varied, from a fairly loose conglomeration of many-flowered primary capitula to a tightly fused structure of one-flowered primary capitula. Regardless, floral initiation proceeds acropetally, while development and anthesis take place basipetally. Secondarily condensed heads have evolved independently also, as is evident in their varied expression across unrelated taxa.

Tertiarily condensed heads are much rarer in distribution, but examples of taxa displaying such inflorescences are found in the Asteraceae, Calyceraceae, Adoxaceae, Dipsacaceae, and Brunoniaceae. The occurrence of the tertiary condensation is correlated with a one-flowered state of the primary capitula. Initiation of the SSPs occurs acropetally on the inflorescence meristem. Each SSP will develop basipetally, with all of the SSPs on the syncephalium initiating simultaneously. Anthesis takes place in the same pattern, which is often unremarked and taken to be random or chaotic.

V. Acknowledgments

I am grateful to Melanie L. DeVore and Michael C. Wiemann for providing the preserved material used in this study.

VI. Literature Cited

Battjes, J. 1994. Determination of organ numbers during inflorescence development of Microseris (Asteraceae: Lactuceae). Ph.D. dissertation, Universiteit van Amsterdam.

Bremer, K. 1994. Asteraceae cladistics and classification. Timber Press, Portland, OR.

Burtt, B. L. 1977. Aspects of diversification in the capitulum. Pp . 41-59 in V. H. Heywood, J. B. Harborne & B. L. Turner (eds.), The biology and chemistry of the Compositae Academic Press, London.

Carolin, R. C. 1978. The systematic relationships of Brunonia. Brunonia 1: 9-29.

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 Species examined in the current study
Family: Species Herbarium [Collector.sup.1] #
Asteraceae
 Palafoxia calosa (Nutt.) T. & G. LSU EMH 375
 Bidens pilosa L. [CR.sup.2] MCW L20
Calyceraceae
 Calycera herbacea Cav. OSU MLD 1206
 Calycera leucanthema (Poepp. OSU MLD 1143
 ex Less.) O. Ktze
Apiaceae
 Eryngium carlinne Delar. [CR.sup.2] MCW L18
Lobeliaceae
 Lobelia tupa L. LSU EMH 764
Family: Species Location
Asteraceae
 Palafoxia calosa (Nutt.) T. & G. Allen Parish, LA
 Bidens pilosa L. San Jose, Costa Rica
Calyceraceae
 Calycera herbacea Cav. Laguna de Manle, Chile
 Calycera leucanthema (Poepp. Talca, Chile
 ex Less.) O. Ktze
Apiaceae
 Eryngium carlinne Delar. Cartago, Costa Rica
Lobeliaceae
 Lobelia tupa L. U.C. Berkeley Bot. Gardens,
 #83.356; orig. Chile
 Distribution of capitula in the Magnoliopsida
 (Classification according to Cronquist, 1982)
Subclass Order Family
Magnoliidae Piperales Chloranthaceae
Hamamelidae Hamamelidales Platanaceae
 Urticales Moraceae
 Casuarinales Casuarinaceae
Caryophyllidae Caryophyllales Nyctaginaceae
 Portulacaceae
Dilleniidae Violales Flacourtiaceae
 Violaceae
 Ericales Empetraceae
 Primulales Primulaceae
Rosidae Rosales Cunoniaceae
 Bruniaceae
 Fabales Mimosaceae
 Fabaceae
 Proteales Proteaceac
 Myrtales Combretaceae
 Cornales Nyssaceae
 Euphorbiales Buxaceae
 Sapindales Burseraceae
 Apiales Araliaceae
 Apiaceae
Asteridae Plantaginales Plantaginaceac
 Scrophulariales Globulariaceae
 Campanulales Campanulaceae
 Brunoniaceae
 Goodeniaceae
 Dipsacales Adoxaceae
 Dipsacaceae
 Calycerales Calyceraceae
 Asterales Asteraceae
 Distribution of territary capitula
 in the Asteraceae
Subfamily Tribe Genus Number of species
Cichorioideae
 Vernonieae Paralychnophora 2
 Arctoteae Platycarpha 4
 Gundelia 2
Asteroideae
 Heliantheae Lagascea 8
 Comparison of primary and higher-order
 inflorescences
 Degree of inflore-
 scence condensation
 Primary
1. Presence of a terminal structure: No truly terminal
 structure
2. Order of anthesis: Acropetal (= centripetal)
3. Order of floral initiation: More or less
 acropetal
4. Order of floral development: More or less
 acropetal
5. Reduction to single, single- Never
 flowered heads:
 Secondary
1. Presence of a terminal structure: At apex of entire
 syncephalium
2. Order of anthesis: Basipetal
3. Order of floral initiation: Acropetal
4. Order of floral development: Basipetal
5. Reduction to single, single- Occasionally
 flowered heads:
 Tertiary
1. Presence of a terminal structure: At apex of syncephalium and
 at apices of individual SSPs
2. Order of anthesis: Basipetal in each SSP; SSPs
 overall simultaenous
3. Order of floral initiation: Basipetal in each SSP; SSPs
 overall acropetal or simultaneous
4. Order of floral development: Basipetal in each SSP; SSPs
 overall acropetal or simultaneous
5. Reduction to single, single- Almost always
 flowered heads:
 Distribution of secondary capitula in
 the Asteraceae (Classification
 according to Bremer, 1994
Subfamily Tribe Number of genera
Barnadesioideae
 Barnadesiae 1
Cichorioideae
 Mutisieae 4
 Cardueae 2
 Lactuceae 3
 Vernonieae 11
Asteroideae
 Plucheae 5
 Gnaphalieae 30
 Heliantheae 9
 Total 65
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Author:HARRIS, ELIZABETH M.
Publication:The Botanical Review
Geographic Code:1USA
Date:Oct 1, 1999
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