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Staminodes: Their morphological and evolutionary significance.

II. Introduction

For the majority of the angiosperms the functional stamen is differentiated into a basal supportive part, namely the filament, and upper microsporangia-bearing tissue, namely the anther (see, e.g., D'Arcy, 1996; Endress, 1994; Endress & Stumpf, 1990, 1991; Hufford & Endress, 1989; Weberling, 1989). Each anther consists of two equivalent halves, the thecae, joined together and with the filament by a connective. Each theca is built up of two pollen sacs (microsporangia), dehiscing in various ways. When stamens fail to develop into the above-mentioned sporogenous structures but retain the same characteristics of microsporophylls, they are usually referred to as sterile stamens or staminodes (e.g., Eames, 1961; Weberling, 1989).

Different definitions can be applied for staminodes. For Watson and Dallwitz (1992-), a staminode is a sterile stamen, or a modified structure identifiable as such, borne in the androecial region of the flower. It may be merely imperfect, vestigial, or specialized (e.g., petaloid or nectariferous). For Mione and Bogle (1990: 78), studying Hamamelidaceae, staminodes are "sterile floral appendages which are most certainly derived from stamens, i.e., appendages which are morphologically similar to stamens but are sterile."

The identification and description of a staminode often remains vague and arbitrary, and may overlap a whole range of different structures: It is an abstraction of something that is neither a stamen (except for those cases with clearly abortive anthers), nor a petal proper, nor any other clearly distinguishable organ. It is clear that, when a stamen aborts, the resulting structure should obviously be called a staminode. This is important for recognizing evolutionary trends in flowers, as the staminode represents a transitional phase from one category of organs to a totally different structure. Difficulties arise when there is absolutely no resemblance between the sterile structure and the fertile stamen. To interpret staminodes in an unequivocal way-like any other floral organ-necessitates a clear-cut approach of homology. For this purpose positional homology should be of major importance in the study of the morphology of staminodes. Staminodes may occur in the same whorl as fertile stamens, as a result of nu tritional limitations (e.g., Baillon, 1862b; Fukuoka et al., 1986) or as the result of a zygomorphic development of the flower (e.g., in many Scrophulariaceae: Endress, 1998, 1999; Reeves & Olmstead, 1998; Table II). An organ that shows no resemblance whatsoever to a stamen may be homotopic; that is, it takes the space in the flower usually reserved for members of the androecium but lacks all resemblance with stamens on a structural ground, even being restricted to vascular bundles, or is totally different in physionomy. The question is whether that organ can always be considered homologous with the stamen. This question cannot be answered positively in all cases, as the homology criteria of Remane (1952, in Sattler, 1994) remain arbitrary. The similarity criterion proposed by Patterson (1982), referring to a combination of topographic, ontogenetic, and compositional homology, was partly taken over by Albert et al. (1998), who distinguished between historical (having a single origin on a phylogenetic tree), p ositional (originating from the same organs), and process homology (having arisen by the same genetic process). The three definitions of homology used by Albert et al. 1998 (also called "orthology") apply to separate organismic levels (organisms, organ primordia, and genes) and may have different applications when discussed for the different levels separately. Ontogenetic homology, referring to a similar ontogeny of stamen and potential staminode (e.g., Kluge, 1988; Nelson, 1978) is another approach combining the historical, positional and process homology, where the staminode is a specialization appearing at one stage in the ontogeny of an organism. According to Sattler (1994) a 1:1 correspondence between structures that is the theoretical (static) criterion for homology is untenable and oversimplified, because of transformations of structures during development ("developmental hybridization") and the occurrence of homeosis, which may be partial or complete. Characters must be compared at all stages of devel opment, and because they eventually become transformed, partial correspondences and multiple relations must be taken into account. This leads to conflicts of homological interpretation, which are only resolved by a dynamic approach of morphology.

The definition of staminodes also implies the presence of heterotopic structures. A typical example of heterotopic staminodes are petals, if petals are considered a category different from the androecium. There is a broad literature covering the homologous nature of petals with stamens, as the subject has fascinated botanists since Goethe (see Weberling, 1989, for an overview). It is undeniable that petals often represent structures reminiscent of stamens and that there is a strong vascular and ontogenetic correlation between the petals and the stamens (see also Albert et al., 1998; Eames, 1931; Endress, 1994; Weberling, 1989). Staminodes can be seen as partially homeotic mutations. They develop from normal stamen primordia but have undergone altered developmental processes and patterns (Li & Johnston, 2000). The development of petals has gone a step farther by the onset of a novel developmental pathway. We could term this transformation from stamen to staminode, and to petal, "serial homeosis," but not in th e sense of Takahashi (1994). Takahashi (1994) proposed this term for the homeotic process occurring in the apetalous flower of Trillium apetalon (Trilliaceae), where there is a serial replacement of organ whorls from the center of the flower to the periphery.

Structures in flowers have often been described as staminodes either because of their superficial resemblance to stamens or because of their spatial association with the stamens. Indeed, it is sometimes very difficult to distinguish between structures that look like staminodes but are not homologous with stamens and those that are derived from stamens. As those structures have often been described as staminodes in the literature, the resulting misinterpretations can have far-reaching consequences for the definition of character states used in data matrices, and they can mislead hypothetical semophyleses of the androecium. It is clear that :he interpretation of staminodial structures meets the same difficulties as the definition of the nature of nectaries and demands a clear-cut characterization (e.g., Ronse Decraene & Smets, 1991c; Smets, 1986, 1988a, 1988b; Smets & Cresens, 1988).

Walker-Larsen and Harder (2000) recently presented a handsome survey of staminodial structures in the angiosperms. They discussed the possible origins of staminodial structures as the result of reductive processes in the androecium using the phylogenetic framework of angiosperm evolution presented by Chase et al. (1993). Patterns of staminode formation are intricately linked to patterns of evolution of whole floral structures. Therefore, staminodes will have different positions and functions in acyclic magnoliids, polysymmetric rosids, or zygomorphic asterids. The authors point to the functional integration of staminodes in the flower of many groups, as we will also discuss below. Shortcomings of their approach are caused by their reliance on literature citations about staminodes and also on certain shortcomings of the phylogenetic hypotheses they use to discuss staminode evolution.

In this article we present a survey of the occurrence of staminodial structures and their functionality in the flower and give an overview of possible misinterpretations of staminodes and their relevance in morphological studies. The difficulty of definition of a staminode may rest on uncertainty in interpreting the wide array of emergences on the floral receptacle. Therefore, a global morphological study, relying on floral anatomy, ontogeny, and external morphology, is needed to clarify this question. We consider staminodes only in hermaphroditic flowers, for the same reasons as given by Walker-Larsen and Harder (2000), because the origin and scope of these staminodes is different for unisexual flowers.

III. Possible Origins for Staminodes

Staminodes appear relatively early in the fossil record, and the same variations as in modern angiosperms seem to have been present since the Turonian. Apart from magnoliid fossils having inner and outer staminodes, there is an abundance of eudicots having one whorl of sterile stamens. They occur in Hamamelidae as a whorl alternating with antesepalous stamens, suggesting their homology with petals and as "a transitional stage between apetalous and petalous flowers" (Grepet & Nixon, 1996: 37). Also in Gapparales-like fossils, such as Dressiantha, five setiform staminodes alternate with five stamens (Gandolfo et al., 1998). Crepet & Nixon (1996) report the presence of antepetalous staminodial nectaries in flowers of Ericalean/Ebenalean affinity. They also suggest that staminodes are responsible for the derivation of nectaries and petals within the rosid-hamamelid complex by a "division of labor" in the stamens. In the ranunculids, staminodes and petals have been derived several times from stamens in separate li neages (see Drinnan et al., 1994).

Several functional explanations have been given for the origin of staminodial structures in flowers linked to evolutionary modifications of flowers (see Walker-Larsen & Harder, 2000). Staminodes may result from nutrient limitations, alterations in the construction of flowers, or adaptations to pollinators. However, different factors may contribute en masse to the elaboration of staminodes.

For obvious nutritional limitations, an entire whorl of stamens may become reduced or may completely disappear. This is illustrated by Rodriguez-Riano et al. (1999) in southwest European Fabaceae, where the incidence of reduced diadelphous androecia is correlated with an autogamous syndrome. In several taxa an inner stamen whorl (usually the antepetalous whorl) may be present, vestigial, or even absent within a single species or between different species of the same genus (Table I). Very often the upper flowers of a racemose inflorescence will not attain full development, leading to a partial sterilization of whorls. This process of reduction, once settled genetically, has affected several lineages of the angiosperms and has arisen several times independently (see Walker-Larsen & Harder, 2000). The process is consistent with the fossil record with the profusion of taxa that have apparent staminodial nectaries (Crepet & Nixon, 1996). The shape of these staminodes is characteristically stublike or sometimes not exceeding the stage of primordium (e.g., Figs. 2-3, 17-19, Myrsine africana, Samolus valerandi, Moringa, Linum). Walker-Larsen and Harder (2000) consider such nonfunctional staminodes temporary and doomed to be lost quickly. However, such structures may have a function in the flower that we do not grasp at this moment.

The trends in the reductive process of stamens (staminode origin) are understood as a semophyletic sequence that can still be traced in certain groups of plants. A reduction in size of stamens, correlated with a retardation of initiation of primordia, can be seen as a first obvious step in the process (Fig. 54). That one of two whorls is often retarded developmentally in diplostemonous flowers has been illustrated (see Ronse Decraene, 1992; Ronse Decraene & Smets, 1995a, 1998; Walker-Larsen & Harder, 2000). The occurrence of obdiplostemony with positional shifts of stamens is one of the mechanisms bringing about the reduction of one whorl in correlation with limitations in time and space for development (Ronse Decraene & Smets, 1995a). These reductive trends have phylogenetic implications as they are correlated with the configuration of the androecium in the eudicots: Diplostemony predominates, but there is a global trend to haplostemony or obhaplostemony. In some genera, species with staminodes coexist with species that have lost staminodes altogether (e.g., Linum, Hesperolinon: Narayana & Rao, 1976a, Samolus: Cans, 1998; Sattler, 1962).

In the monocots similar reductive trends are operating. The Zingiberales are a classic example of the semophyletic sequence in stamen reduction from an original dicyclic androecium running in a continuous sequence (the reductive process is represented with symbols used for floral formulas; A refers to the androecium, the numbers refer to the number of stamens in a whorl, and the raised circle refers to staminodes): Musaceae [A3+3 or A3+2(1[degrees]) / Heliconiaceae [A2(1[degrees])+3] - Lowiaceae / Strelitziaceae (A3+2) - Zingiberaceae [A2[degrees]+ 1(2[degrees])] / Marantacene [A1[degrees]/2[degrees]/0+1(2[degrees])] - Costaceae [A3[degrees]+1(2[degrees])] - Cannaceae [A2[degrees]+(2[degrees])] (see, e.g., Kirchoff, 1991; Kress, 1990). These reductions are correlated with a trend from small vestigial organs to specialized pollination mechanisms (pollinator attraction, trigger mechanisms, pollinator guidance: Endress, 1994, Walker-Larsen & Harder, 2000). The process of staminode formation must be seen as the o ngoing interaction of heterochrony and heterotopy. Heterochrony changes the developmental timing and rate of development of the organ, without changing the developmental direction; heterotopy changes the nature of the organs formed, not the timing and rate of morphogenesis (Li & Johnston, 2000).

In a first evolutionary step staminodes are incidental and must be seen as a response of the flower to a changing external or internal condition. For example, a trend to zygomorphy induces one side of the flower to become retarded in its development relative to the opposite side (e.g., Leguminosae: Tucker, 1984, 1996; Moringaceae: Ronse Decraene et al., 1998a). This leads to a retardation versus stagnation in inception of part of the androecium and finally to its sterilization or abortion. This shift to sterility can run from the adaxial side to the abaxial side; Emblingia has four adaxial stamens opposite the petals and four abaxial staminodes (Erdtman et al., 1969). The opposite occurs in Dactylaena and Euadenia (Gapparaceae), in which four adaxial staminodes fuse into a stalked appendage facing the single abaxial stamen (Figs. 4-5; Karrer, 1991). Different reductive trends may be correlated in one flower, as in Moringa (Ronse Decraene et al., 1998a). A generalized feature in the genus is that the antepetal ous stamen whorl is reduced to stublike staminodes with no obvious function. The flower also develops a strong oblique zygomorphy. As a result, one of the staminodes is much smaller than the others and is sometimes absent (Figs. 1-2; see Ronse Decraene et al., 1998a). The duality between two groups of stamens (heteranthery) is a frequently recurring pattern related to pollination and is one probable origin of staminodes in zygomorphic flowers. Pollen flowers with some feeding stamens and only a small number of larger pollinating stamens are characteristically arranged in two opposing groups in a monosymmetric pattern (see Endress, 1999; Vogel, 1978). The feeding stamens either produce either nonviable pollen or ultimately become completely sterile.

In a second step (probably simultaneously with the loss of pollen-producing activities), these retarded organs can become transformed (by a reversal of the original strictly reductive trend) and may gain another function in the flower. Statements of functionality versus nonfunctionality are sometimes dubious, as very little is known of the floral biology of flowers. Such alternations of trends are clearly very dynamic and are related to several internal (e.g., the degree of sterilization, occurrence of homeosis) or external factors (e.g., pollinator- flower relationships). It is essential that a genetic basis exist for a reprogramming of a moribund staminodial structure; otherwise, the staminode is doomed to disappear quickly. However, one can argue whether a stublike structure should still be present in flowers when it has no obvious function. At the same time it is an indication of an ongoing evolutionary process (He [beta], 1983). In the zygomorphic Scrophulariaceae the adaxial staminode can be variously d eveloped, may vanish completely, or be sometimes conspicuous (see Endress, 1998, 1999; Reeves & Olmstead, 1998; Walker-Larsen & Harder, 2000).

Table II illustrates the strong link between zygomorphy and the occurrence of adaxial staminodes spread over different genera Notable exceptions with anterior staminodes are Emblingia (Erdtman et al., 1969), Lopezia (Eyde & Morgan, 1973), and Pelargonium (Kumar, 1976; Sattler, 1973). The siting of staminode formation is linked to such factors as the orientation of the flower on the inflorescence and the type of visiting pollinator. The development of staminodes in zygomorphic flowers is independent of the number of stamen whorls, reflecting a different gene expression.

IV. A Redefinition of Staminodial Structures

A. SURVEY OF THE PROBLEM: SOME CASE STUDIES

Character research implies that characters are selected for their systematic value and their consistency (absence of homoplasy) in phylogenetic analyses. As staminodes are integral part of the androecium, they are involved in definitions, related to topologies of the androecium (see, e.g., Ronse Decraene & Smets, 1993, 1995a, 1998). Predominating ideas or theories of floral evolution have influenced the approach of the androecium and staminodes in particular. As staminodes are by definition vestigial structures, they have been linked to a reductive process in flowers, along the lines of the ranalean theory. This has repercussions on descriptions of "vascular stubs" that occur on the receptacle and that are related with preexisting staminal whorls. Also, reports on the presence versus absence of vascularization in staminodes are often contradictory. In this article we demonstrate that staminodes can be confounded with all sorts of structures. Therefore, a careful study of their nature is required, involving an atomical, ontogenetic, and--if possible--genetic investigations. It should be stressed here that the circumscription of floral characters in a hierarchical ordering of characters and character-states remains a necessity for all phylogenetic analyses and that staminodes must also be approached in this way (Table I). The difficulty in interpreting staminodial structures can be illustrated by following examples:

1. The flower of the monotypic genus Corynocarpus J. R. & G. Forst. (Corynocarpaceae) has a perianth differentiated as five sepals and petals and an androecium of five antepetalous stamens, alternating with antesepalous scales bearing a ventral nectary (Figs. 7-8). In the past, different interpretations have been given for the petaloid antesepalous scales. Krause (1960), among others, considered the scales staminodes and the nectaries opposite these scales a disk (namely, receptacular outgrowth). Narayana et al. (1986) interpreted the scale and nectary as part of a single staminodial structure; the nectary represents the modified anther part and the petal-like scale equals the transformed connective. Another interpretation, formulated by Philipson (1987), represented the petaloid scales as equivalent to petals and the nectaries as staminodes, not as a disk. However, he admitted that the common vasculature of scale and nectary could be an indication of a strong relation between "petal" and scale. Nonetheless, scarce ontogenetic evidence seemed to suggest that "it is not possible to distinguish between the primordia of petals and scales, nor between those of stamens and nectaries" (Philipson, 1987:13). In the absence of any clear evidence, Philipson opted for avoiding the use of the term "staminode" and preferred terms such as "petaloid scale" and "nectary" instead. The interpretation of Krause (1960) is supported by the fact that the nectary is inserted lower on the hypanthial slope and has no vascular connection (Ronse Decraene, unpubl. obs.). A thorough ontogenetic study should give more evidence of the nature of staminode and nectary, as the morphological evidence is still uncertain.

(2.) Harungana madagascariensis (Glusiaceae) and several other Clusiaceae possess antepetalous stamen fascicles alternating with five indented nectary scales (Fig. 9). Although the scales arise relatively late in ontogeny and have occasionally been interpreted as receptacular emergences (e.g., Leins, 1964), they are supplied by massive bundles alternating with the stamen traces and look superficially like anthers (Fig. 9). On this evidence Ronse Decraene & Smets (1991a) concluded that the nectaries represent a second staminodial whorl. In other taxa in which the presence of staminodes is beyond discussion (e.g., Samolus in Primulaceae) the staminodes also arise at a very late stage of development but are without vascular tissue (Caris, 1998; Ronse Decraene & Smets, 1995a).

(3.) Greyiaceae and Francoaceae have been shown to be closely related on the basis of rbcL data (e.g., Chase et al., 1993; Morgan & Soltis, 1993) and ontogenetic evidence (e.g., Ronse Decraene & Smets, 1999). Both families have interstaminal emergences that resemble staminodes and have been described repeatedly as such in the literature (e.g., Bensel & Palser, 1975b; Cronquist, 1981; Dahlgren & van Wyk, 1988; Morgan & Soltis, 1993; Takhtajan, 1997). Ontogenetic and anatomical studies have shown that these emergences represent nectaries with a receptacular origin and without vascular connection, and that they are not homologous with the stamens (Figs. 10-11; e.g., Klopfer, 1972; Payer, 1857; Ronse Decraene & Smets, 1999).

(4.) Staminodes in a similar antepetalous position either are vascularized (e.g., Erodium) or are not vascularized (e.g., Linum). For some taxa, reports are contradictory (e.g., Erodium: Figs. 12-13, Averrhoa: Fig. 14; Al-Nowaihi & Khalifa, 1971; Kumar, 1976; Narayana, 1966). For example, Al-Nowaihi & Khalifa (1973) consider the antepetalous "teeth" of Linaceae ligular appendages, not staminodes, because they lack vascularization. Indeed, other studies in Linaceae (e.g., Narayana, 1964; Narayana & Rao, 1976a, 1976b, 1977a, 1977c) report the absence of vascularization, except for Kumar (1976), mentioning short vascular stubs leading to the staminodes in Linum. The presence of antepetalous staminodes, together with antesepalous nectaries against the stamens in Erodium (Figs. 12-14), led to even more imaginative interpretations. Dawson (1936) and Kumar(1976) interpreted the androecium of Geraniales as originally triplostemonous with a progressive reduction series, leading to the transformation of outer antesepal ous stamens into glands and antepetalous stamens into scale-like staminodes. However, the staminodial nature of the nectary was put in doubt by Al-Nowaihi & Khalifa (1971) because of the absence of any vascularization. It is clear that the nectaries in Erodium have nothing to do with the staminodes and arise independently (Figs. 12-13). In Averrhoa, nectaries and staminodes occur as undistinguishable structures that are vascularized (Fig. 14). The presence of an intrastaminal disk, together with a whorl of vascularized staminodes (as in Toona, Cedrela of Meliaceae and Flindersia of Rutaceae: Sheela Lal, 1994; Sheela Lal & Narayana, 1994), makes the interpretation of staminodes more concordant among authors. In Cedrela the antepetalous stamens are suppressed, but their traces persist within the receptacle. The related genus Toona has persistent staminodes (Baillon, 1895; Harms, 1960).

(5.) In the Hamamelidaceae it is difficult to distinguish among sterile phyllomes or appendages, staminodes, and nectaries. In Hamamelis, Mione and Bogle (1990) describe an antepetalous whorl as nectary primordia, while they describe the homotopic antepetalous whorl of Loropetalum as sterile phyllomes. In both taxa the sterile structures occasionally develop as staminodes, suggesting a staminodial origin (Baillon, 1871; Mione & Bogle, 1990). Sterile phyllomes similar to those of Loropetalum occur in other genera of Hamamelidaceae (Rhodoleia, Corylopsis: see Bogle, 1989; Endress, 1967; Figs. 15-16). Mione and Bogle (1990) argue that the sterile phyllomes of Loropetalum, nectaries of Hamamelis, and staminodes of Corylopsis are not derived from the same whorl of organs, because they do not arise at similar times in the development of the flower, because they have a different vascular connection, and because the least specialized genera, Maingaya and Dicoryphe, bear two whorls of both staminodes and sterile phyll omes with a different vascular supply. These facts indicate that progenitors of subfamily Hamamelidoideae of Hamamelidaceae probably possessed an androecium with at least three whorls with a functional divergence of nectariferous staminodes and sterile structures (cf. Bogle, 1989; Mione & Bogle, 1990).

From these examples it is clear that a topological definition for a staminode is sometimes sufficient but that in other cases it is not. In the example of Harungana, the topological criterion is supported by the vasculature and by the shape of the nectary. In Greyia and Francoa the stublike structures are associated with the androecium and alternate with the stamens, but they have nothing in common with staminodes. Indeed, the acceptance of the nectarial stubs as staminodes involves the acceptance of ancestral polyandry in Greyiaceae and Francoaceae, where the related rosid families are all basically diplostemonous.

The characterization of sterile stamens (i.e., staminodial structures) should be based on a combination of function and position in the flower rather than on their external morphology, as they are derived from a nonfunctioning stamen that must have preceded them in evolution (Figs. 52-54). Contrary to fertile stamens that are more or less restricted in their external morphology by their limited pollen-providing function, staminodes have evolved in a great variety of shapes, because of their varied functions, obscuring patterns of homology. The presence of vascular connections and the development of primordia are helpful tools for differentiating a staminodial structure. Therefore, we propose to characterize staminodes in two ways: a functional definition, with a major distinction between vestigial staminodes and functional staminodes (Fig. 52); and a topological definition, in which staminodes are approached on the basis of their relationship with the other organs in the flower (Fig. 53). The functional appro ach and topological definition can be combined in a time-related model, in which the evolution of the staminodes over time is stressed (Fig. 54).

Staminode evolution should be read as a progressive transformation series running from a fertile stamen into highly specialized forms. It runs from an imperfect, sterile stamen into a regressing or vestigial organ. Further evolution is biased between total loss and a conversion into a novel structure. Topology-based and function-based definitions are essentially hierarchical, in that a staminode either is homologous with a whole stamen or is part of an organ. As the androecium arises in a sequence in the flower, which may be spiral or whorled, a more detailed definition implies that the outer sphere (toward the perianth) has a staminodial nature (petalostaminodia) or that intervening (inner or middle) sterile whorls (antepetalous or antesepalous) are described as staminodial. Staminodes may also exist within a whorl or in a closed series. Staminodes as partial organs imply that they arise by the division of a common primordium.

B. EVOLUTION OF STAMINODIAL STRUCTURES: FUNCTION-BASED DEFINITION

1. Vestigial Staminodes

In its simplest form and as a primary step in stamen reduction, staminodes can persist as regressing or vestigial organs in the flower. Staminodes are an indication of a changing process, namely a reductive trend, either by the loss of a whole whorl of stamens in the transition from diplostemony to (ob)haplostemony (e.g., in Sterculiaceae, Geraniaceae, Primulaceae, Mytraceae; Ronse Decraene & Smets, 1995a; Figs. 12, 15; Table I) or by the partial reduction of stamens within a whorl (in relation to zygomorphy: e.g., in Scrophulariaceae, Verbenaceae: see Endress, 1999; Ronse Decraene & Smets, 1994, 1995a; Walker-Larsen & Harder, 2000; Figs. 20-21; Table II). Such structures can be defined as "vestigial staminodes." Although the extent of reduction differs, they are fundamentally little altered morphologically in comparison to fertile stamens. Such staminodes may possibly retain their vasculature (helping in their identification as staminodes), or the vasculature may fade out before reaching the organ or be lost completely (e.g., Euadenia: Arber, 1933; Raghavan, 1939). These staminodes may have a function in the flower, but this is not always clear.

Vestigial staminodes may be found at different stages of reduction, namely as a whorl of sterile stamens with small apical anthers (which are occasionally fertile) (e.g., Manilkara: Pennington, 1991; Anacardium: Figs. 20-21), as filaments without anthers (Paronychia: Figs. 17-19), as more or less small stubs (e.g., Anthirrhinum, Sagina, Moringa: Figs. 1-3), or as minute organs that appear in the early ontogeny of the flower but are no longer visible at maturity (e.g., Digitalis: Chatin, 1873a; Singh, 1979). Such staminodes may be initiated as a regular whorl of stamen primordia but abort at a certain stage of their development (e.g., Cedrela [Toona]: Baillon, 1895). However, the regular alternation of whorls may often become disturbed when the sterile structures arise after the fertile whorl, as is the case for centrifugal obdiplostemony (e.g., Theobroma in Sterculiaceae: Ronse Decraene & Smets, 1995a).

In other cases, staminode initiation is delayed until well after the initiation of the carpels (e.g., Paronychia decandra: Fig. 17; Samolus valerandi, Magodendron: Ronse Decraene & Smets, 1995a; Vink, 1995). Theophrastaceae, Sapotaceae, Myrsinaceae, and Primulaceae are examples of the derivation of the obhaplostemonous androecium from diplostemonous ancestors. Although all Theophrastaceae possess colored, attractive staminodes little different from petals, some genera of Myrsinaceae (e.g., Myrsine), and Primulaceae (e.g., Samolus) possess evidence of antesepalous staminodes: In all cases the staminodes arise after the initiation of the common stamen-petal primordia (Caris, 1998).

It is possible that a stamen or a whole stamen whorl has vanished externally but that evidence of residual traces persists internally. For example, in the Primulaceac the median sepal traces split tangentially and give off five internal traces, which alternate with the common stamen-petal traces. They appear in the petal tube as the fused petal marginals. In Steronema these bundles split twice, providing the petal marginal bundles and "staminodium" bundles, which come to lie in a ring with the stamens (Douglas, 1936). This induced certain authors to consider these marginal petal traces transformed stamen traces (e.g., Soldanella: Saunders, 1937-1939; Primula. Subrarnanyam & Narayana, 1976). Although this evidence appears to be a point for those who advocate vascular conservatism, it is absolutely not proof of a staminodial origin (see also Arber, 1933; Schmid, 1972).

In Mangifera indica L. or Anacardium occidentale L. (Anacardiaceae), reductions have affected the whole antepetalous whorl and four stamens of the antesepalous whorl (Figs.20-21). The antepetalous whorl may often be wholly suppressed, apart from the occasional presence of short vascular traces (Sharma, 1954); the single fertile antesepalous stamen receives a larger trace than do the sterile antesepalous stamens.

The abortion of stamens within a whorl can affect different halves of the flower, with intermediate half-fertile anthers in the genera Conospermum and Synaphea (Proteaceae). The configuration of the androecium is mirror imaged between the genera, with an adaxial (Synaphea) or abaxial (Conospermum) sterile anther and two lateral anthers with one half sterile (Douglas, 1997).

2. Functional Staminodes

In several instances staminodes have become adapted to fulfil novel biological requirements in the flower in response to a specific pollination syndrome. Petals (petalostaminodia or andropetals) also play that role, but most often in a more generalized way.

The different functions of staminodes can be summarized as follows (Fig. 53):

* Production of a food supply (nutrient bodies, sterile pollen, or nectar): nutritional function;

* Development of collecting structures in association with nectaries (as nectar recipients), triggering mechanisms for pollen dispersal, secondary pollen presenters, obstacles for selfing: structural function;

* Attraction of pollinators by display of colors, odors, or heat: attractive function.

Staminodes may fulfill several functions at the same time, namely producing nectar, collecting or holding it, and being optically attractive (e.g., Parnassia), or different sets of staminodes may have different functions in the same flower (e.g., inner versus outer staminodes in Himantandraceae: Endress, 1984, 1986). In the magnoliids the staminodes have multiple functions related to pollination, such as attracting and directing pollinators by their color, odor, food supply, and secretions, protecting the ovary against predation, effecting pollination or preventing selfing by their position or by movements, or providing shelter and warmth (Endress, 1984, 1994; Thien et al., 1999; Walker-Larsen & Harder, 2000).

The transition from nonfunctional sterile stamens to nectar-producing structures is apparently relatively easy, depending on a vascular connection, as in Azara (Flacourtiaceae), where the short stubs produce nectar through stomata (Figs. 36-37). In Loasaceae (subfamily Loasoideae) the antesepalous stamens have become differentiated into colored nectar recipients (Figs. 29-30; Hufford, 1990; Smets, 1988a, 1988b; Urban, 1892). For example, in Loasa (Loasaceae) the staminodes are bright yellow and red, contrasting with the white corolla. In Harungana madagascariensis (Choisy) Poir. (Clusiaceae) the antesepalous stamen whorl has become transformed into scale-like nectaries (Ronse Decraene & Smets, 1991 a; Fig. 9). In the genera Piciarium and Archytaea of Bonnetiaceae, nectaries are discrete, antepetalous structures alternating with the stamen clusters that are supplied by double bundles similar to stamens (Dickison & Weitzman, 1998). In certain families, such as Aizoaceae, part of the centrifugally developing sta mens grow into colored staminodes (Hofmann, 1993; Ihlenfeldt, 1960). Parnassia (Parnassiaceae) has a whorl of antesepalous stamens alternating with staminodial nectaries and resembling a fascicle of sterile stamens (He[beta], 1983). Floral anatomy and ontogeny demonstrate that the nectaries are equivalent to single reduced stamens (see Bensel & Palser, 1975a; Klopfer, 1972; Saxena, 1976).

These examples of staminodes are transformed structures, namely they are basically homologous to stamens, but they have been altered by their functional requirements. Because of their obvious role in the flower, contrary to vestigial staminodes, we prefer to describe this type of sterile structures as "functional staminodes."

C. STRUCTURAL SIGNIFICANCE OF STAMINODIAL STRUCTURES: TYPOLOGY-BASED DEFINITION

1. Acyclic Staminodes

Primitive taxa of the Magnoliidae often possess staminodial structures between stamens and tepals and between carpels and stamens (e.g., Bernhardt, 1996; Endress, 1984, 1986, 1990a, 1990b; Ronse Decraene & Smets, 1993; Walker-Larsen & Harder, 2000). These staminodes are typical of spiral flowers with little or no synorganization. They represent stepping stones between different organs (e.g., tepals-stamens-carpels) and have occasionally attained specific (overlapping) functions in the flower.

For Eames (1961), the first mode of attraction of the angiosperms consisted exclusively of these upper staminodes (Figs. 32-33). However, such cases are isolated and are not linked to the generalized condition with staminodes situated in the periphery of the flower. The initiation of floral organs in a close helical sequence leaves little space for differentiation between distinct groups of floral organs without disturbing the helix considerably. The transition between tepals, sepals, petals, and stamens can only be a gradual process in this case, in which staminodes play an important role as multifunctional transitional structures (e.g., protective structures versus nutrient bodies or showy attractive organs: see Endress, 1984, 1986, 1990a). In the eudicots the different functions often become separated in space and time.

2. Complete Staminodial Whorls

In many cases (see Table I) a whorl of stamens tends to become completely sterilized in the flower. In this way a diplostemonous androecium becomes transformed into an (ob)haplo-stemonous one. Evidence for a phylogenetic link between the two androecial configurations, running only in one direction, relies essentially on staminodial structures (see Ronse Decraene & Smets, 1995a). Staminodes evolved many times in the rosids (Walker-Larsen & Harder, 2000). In the Malvales and former Theales the occurrence of antesepalous staminodes is correlated with secondary multiplication of the other stamen whorl (Fig. 38). Staminodes tend to be the expression of a no-return reductive process, although they occasionally attain a new function in the flower (e.g., Bonnetiaceae, Clusiaceae, Malvaceae, Sterculiaceae, Parnassiaceae, Lepuropetalaceae: Figs. 2, 7, 9, 12, 15, 36, 38).

Whorls of staminodes related to a reductive trend also occur in the more primitive taxa with a polycyclic androecium. Monanthotaxis whytei (Stapf) Verdc. (Annonaceae) has two outer whorls of staminodes (Ronse Decraene & Smets, 1990a, 1993; Fig. 31). The more external whorl of six pairs appears in early development but is hardly visible at maturity; the next whorl of nine staminodes remains relatively large at maturity. Such cases probably represent stages in a stepwise reduction of a polycyclic androecium (see Ronse Decraene & Smets, 1993).

3. Petalostaminodia

The corolla, or petal whorl, represents a special case of a complete staminodial whorl. Staminodes are sometimes petaloid, leaflike appendages that cannot be differentiated from the petals (e.g., in some Theophrastaceae, Corynocarpaceae: Figs. 7-8). They are evidence of a direct link between stamens and petals. As they are not different from petals or it is in some cases not possible to differentiate them (e.g., in some Caryophyllaceae), this kind of petaloid staminodes are best called "Petalostaminodia." Teratologica] cases of double flowers, as in Rosaceae or Malvaceae (e.g., Innes et al., 1989; Maclntyre & Lacroix, 1996) are a classic example of this transition. In other cases petaloid staminodes may be observed in the position that petals normally occupy (e.g., in Hamamelidaceae: Endress, 1967; Mione & Bogle, 1990, Caryophyllaceae: Ronse Decraene et al., 1998b; Fig. 25). The number of stamens can also be augmented at the cost of petals (Murbeck, 1918: "staminal pseudapetaly," quoted in Endress, 1967).

Petals represent a problematic case of staminodial origin, as it is generally assumed that the petals of a great many angiosperms have been derived from stamens and are homologous with them (e.g., Cronquist, 1988; Eames, 1961; Endress, 1986, 1994; Hiepko, 1965; Takhtajan, 1980, 1991; Weberling, 1989; Worsdell, 1903). In many cases it is difficult to determine when a petal ceases to be a staminode and when a staminode ceases to be a stamen (Figs. 24-25). At another extreme, petals can sometimes attain all structural and developmental attributes of sepals, concomitant with changing functions (Endress, 1994). Strictly speaking, petals must be seen as showy, flattened, and colored organs occupying the space between the sepals and the androecium. In comparison with staminodes within the androecium, the development of petals from stamens is an evolutionary step that has taken place repeatedly in angiosperm evolution.

Petals have probably arisen several times in the Ranunculales from outer (nectar-producing) staminodes (see, e.g., Drinnan et al., 1994; Endress, 1995; Hiepko, 1965; Kosuge, 1994; Figs. 22-23, 34-35). In Ranunculaceae there are transition series from inconspicuous staminodes to elaborate petaloid nectar leaves occurring among genera (Ronse Decraene & Smets, 1995b). The morphological homology between nectar leaves and stamens has been traced back ontogenetically in a number of species of Ranunculaceae by Erbar et al. (1998). A topological definition of staminodes is also in concordance with the nectary types proposed by Smets (1 988a), nectaria nectarophyllomina and nectaria staminodialia. The nectarophyllomina type of nectaries (or Helleborus type) correspond with the petalostaminodes characteristic of the Ranunculales (e.g., Ranunculaceae, Berberidaceae, Menispermaceae). The staminodialia type of nectaries (or Trigonia type) correspond with staminodes that are more strongly associated with the androecium.

Clear ontogenetic descriptions of homeotic shifts between petals and stamens are Sanguinaria, with an extra whorl of petals (Papaveraceae: Lehmann & Sattler, 1993) and Actaea (Ranunculaceae: Lehmann & Sattler, 1994), petals transformed into stamens in Macleaya (Papaveraceae: Ronse Decraene & Smets, 1990b), stamens occupying the position of petals in Saraca and Swartia of the Leguminosae (Tucker, 1988b), Dichapetalum (Dichapetalaceae: Breteler, 1973; Figs. 26-28, but see Table III), or double-flowered Hibiscus of Malvaceae (MacIntyre & Lacroix, 1996). Illustrations of Swartia in Tucker (1988c: 77) show that there are a single petal and three large stamens in one outer whorl, while the remaining stamens are crowded on a ring primordium. The transition of stamens into staminodes, and further into petals is best described by the term "serial homeosis."

The terms "andropetals" (related to and derived from stamens and similar to staminodes) and "bracteopetals" (related to and derived from bracts and sepals) distinguish between two kinds of petals in the angiosperms, even when shifts have occurred between petals and sepals (see Hiepko, 1965; Kosuge, 1993; Ronse Decraene & Smets, 1993, 1995b; Takhtajan, 1991). Important arguments for the presence of "andropetals" as opposed to "bracteopetals" (Hiepko, 1965; Takhtajan, 1991) are the vascular arrangement (one-trace organs; however, this distinction has little relevance because three-traced stamens may also occur), the ontogeny (similarity to stamen primordia in shape of primordia, retardation of growth of the petals), teratological cases, but most important the spatial relation between stamens and petals (existence of parastichies). Very often petals resemble stamens in having a stalk and a limited insertion area (clawed structures). Staminodes belonging to a staminal whorl may also become secondarily petaloid, a s in the Zingiberales (e.g., Kirchoff, 1991; Walker-Larsen & Harder, 2000).

Flowers are occasionally secondarily apetalous but may occasionally become secondarily petaliferous. In that case, outer staminodes may be differentiated as outer petaline structures, which confuses the limits between petals and staminodes as in Scytopetalaceae (Appel, 1996), or there is an outer receptacular corona without clear homology with staminodes (Passifloraceae: Bernhard, 1999a).

The strong link between petals and stamens has a genetic basis that has been extensively studied in the last ten years for the model genera Antirrhinum and Arabidopsis (e.g., Bowman et al., 1991; Coen & Meyerowitz, 1991: ABC model). At the same time, the petals are intermediate between stamens and sepals. We therefore assume that there are repeated evolutionary origins for petals, either from stamens (in the majority of eudicots) or from sepals.

4. Incomplete Staminodial Whorls

The presence of staminodes within a stamen whorl is often an indication of the monosymmetric development of the flower. A stamen whorl becomes partially sterile, as an adaptation to a "vectorized" pollinator visit. The reduced stamen usually occupies a position crossed by the symmetry line. Staminodial structures may be found within one or two whorls of stamens, depending on the androecial configuration that functions as the starting point.

In the Fabales stamens arise unidirectionally, and the abaxial part of the androecium is often "advanced" compared with the posterior part. Adaxial stamens are often smaller, as they lag in development (e.g., Chamaecrista: Tucker, 1996), are staminodial (as in Petalostylis with two antesepalous staminodes: Tucker, 1998; or in Cassia and Senna with three adaxial staminodes and a strong heteranthery: Tucker, 1996), or are missing. An extreme is Bauhinia divaricata, with a single stamen, nine staminodes, and a variable number of petals (Tucker, 1988b). Petals and all other stamen primordia are initiated but are arrested at a given stage of their development. Other species of Bauhinia have a variable number of staminodes, have sterile stamens, or none at all (Tucker, 1984, 1988b).

In many taxa of the asterids, zygomorphy is correlated with the occurrence of an adaxial staminode. Androecial initiation is unidirectional, with a delayed initiation of the adaxial staminode, which may not arise at all in some cases (e.g., Baillon, 1860b, 1862c; Bocquillon, 1861b; Chatin, 1873a; Endress, 1998, 1999; Payer, 1857; Singh & Jain, 1978). The posterior staminodes of many asterids either are small and reduced or can be secondarily increased in size, concomitant with a functional diversification (e.g., Kigelia: Neubauer, 1959; Penstemon, Scrophularia: Endress, 1994). Reductive trends of the posterior stamen in the Verbenaceae can be followed through several intermediates, ranging from the obvious presence of staminodes, to their initiation and consecutive loss and their total absence (Bocquillon, 1861b; Payer, 1857; Sattler, 1973).

The possibility of a reversal of staminodes and the reappearance of fertility has been discussed by Walker-Larsen and Harder (2000) for the Scrophulariales. This reversion is correlated with a transition to radially symmetric flowers. We doubt that this process is possible, because reversals to radially symmetric flowers in asterids operate via the loss of the posterior staminode and the fusion of the posterior petals and the transition to tetramerous flowers (see, e.g., Ronse Decraene & Smets, 1994; Endress, 1999). Loss of stamens seems irreversible, certainly for whole stamen whorls and probably also for reductions within whorls, except for the occasional genetic mutation or monstrosity, unless one considers the event of peloric mutants (e.g., Antirhinum: Coen & Meyerowitz, 1991; Coen et al., 1995) as a leading factor in floral evolution. Although insights into molecular evolution of flower development rest mainly on homeotic mutants, their importance to floral evolution remain virtually unknown (cf. Li & J ohnston, 2000).

5. Secondary Staminodial Structures

In some families with a multistaminate, centrifugal androecium the outer stamen primordia are not developed beyond the stage of antherless structures (e.g., Dilleniaceae: Baillon, 1865, 1866; Endress, 1997; Fumana in Cistaceae: Nandi, 1998; Bixaceae: Ronse Decraene, 1989; Aizoaceae: Hofmann, 1993; Limnocharitaceae: Haynes et al., 1998). The existence of this kind of staminodes is probably linked to the secondary appearance of the centrifugal stamens and is induced by the rapid development of the flower (see Ronse Decraene & Smets, 1992). Centrifugal stamen development lags behind the development of other floral organs, and there is probably not enough time or nutrient allocation to attain a full development of the outermost stamens. Note that the presence of outer staminodes in a polyandrous androecium has often been interpreted as evidence for a reductive trend (see Ronse Decraene & Smets, 1992, 1993). In Paeonia, innermost stamens may be staminodial by pressures of the developing internal disk (Hiepko, 1966 ).

In some cases the outer staminodes of centrifugal androecia have become converted to new functions, linked with pollinator attraction. In Loasaceae subfamily Loasoideae a variable number of antesepalous staminodes develop into colored nectar collectors (Hufford, 1990; Smets, 1988a, 1988b; Figs. 29-30). In Dilleniaceae the outermost stamens may develop into a corona (Pachynema: Endress, 1997). The flowers of Scytopetalaceae are basically apetalous but have a showy corona (pseudocorolla) of staminodial origin (Appel, 1996). In the related Lecythidaceae, external staminodes have evolved in colored, complex structures (Endress, 1994). In Couroupita guianensis the abaxial part of the androecial ring primordium is detached as a broad flap of tissue with numerous staminodes covering the fertile stamens like a hood. This hood may contain fodder staminodes with pollen, or nectar may be produced at the base of the staminodes. Different pollination mechanisms and references hereto are abundantly discussed in Endress (19 94).

Secondary staminodial structures have the same characteristics as secondary stamens arising on common primordia. They may be vestigial or have evolved different functions related to pollination (Fig. 54).

V. Imaginary Staminodes

A. PSEUDOSTAMINODES

The difficulty in interpreting the homology of staminodes has often led to erroneous statements about structures surrounding the androecium. A striking similarity of intrastaminal emergences to filaments, prominent appendages of fused stamen bases, invaginations of the petals, or receptacular emergences, which are sometimes nectariferous, were often taken as evidence of a second aborted stamen whorl. Numerous examples exist in which sterile emergences have been interpreted as staminodes without supporting evidence (see Table III, Figs. 39-40). These appendages commonly arise very late in ontogeny and are not vascularized, or they are vascularized by various means. The following examples illustrate the difficulty in interpreting pseudostaminodial floral appendages:

1. Short-stalked glands occur at the base of the inner staminodes of Gomortegaceae (e.g., Brizicky, 1959) and Hernandiaceae (e.g., Kubitzki, 1969; Sastri, 1965) and on the outer, intermediate, or inner stamens of Lauraceae (e.g., Endress & Hufford, 1989; Kasapligil, 1951; Rohwer, 1994; Sastri, 1965; Vattimo, 1959; Fig. 41) and Monimiaceae (e.g., Endress, 1980; Sampson, 1969). Because the lateral appendages look superficially similar to reduced stamens, most authors have taken the basally inserted nectaries on the stamens of Laurales as evidence of reduced stamen fascicles and have interpreted the nectaries as lateral stamens in a clear state of reduction (e.g., Eames, 1961; Reece, 1939; Rohwer, 1994; Sampson, 1969; Sastri, 1952, 1965). Other evidence, especially a comparison with the lateral androecial lobes of Chloranthus (Chloranthaceae), has been used for arguing a derivation of lauralean stamens from primitively branched structures (Rohwer, 1994). Kasapligil (1951: 182), on the other hand, regarded the st aminal glands as "emergences produced de novo for a functional purpose." He observed that the staminal glands arise late in ontogeny from lateral meristematic regions of the stamens. Other recent observations of the floral ontogeny of the flower of Lauraceae support Kasapligil's view (Endress, 1980; Singh & Singh, 1985), because no difference is found between the early inception of stamens with nectaries and those without nectaries. Moreover, no fasciculate stamens are known in the Laurales, and the relative (vascular) independence of the nectarial appendages is due to their late appearance in ontogeny (Endress, 1980). However, Crane et al. (1994) interpret fossil evidence of a lauralean flower as having an outer whorl of six staminodes, apparently set in three pairs, each of which appears to be linked to a single stamen. Could the fusion of the staminode with a stamen lead to a tripartite structure? The question of paired staminodes is contradicted by a review study by Eklund (2000) of fossil Lauraceae flowe rs which demonstrates a basic and constant pattern of four trimerous stamen whorls, the innermost being staminodial and with only the third bearing paired glandular appendages. The question is clearly not settled, especially in comparison with the tripartite structure of Chloranthus (Chloranthaceae).

2. The intrastaminal appendages between the fused stamen bases of Amaranthaceae have been interpreted either as true staminodes representing a lost stamen whorl (e.g., Goldberg, 1986; Joshi, 1932; Joshi & Venkata Rao, 1934; Saunders, 1937-1939) or as emergences of the staminal tube without clear morphological identity (e.g., Eliasson, 1988; Payer, 1857; Schinz, 1934). Eliasson (1988) observed that broad filaments are correlated with an absence of interstaminal emergences and that small filaments share the presence of pseudostaminodes. The intrastaminal teeth arise late in ontogeny (Payer, 1857) and have no vascular connection (Schinz, 1934).

3. Pseudostaminodes and real staminodes may occur in a same flower, as in Sauvagesia (Ochnaceae), with an outer fringe of threadlike appendages and a whorl of five petaloid staminodes in the petal radii (e.g., Amaral, 1991; Eichler, 1875-1878; Goebel, 1933; Saunders, 1937-1939). Outer staminodes may co-occur with the five antepetalous staminodes (S. erecta), only the antepetalous staminodes may be found (S. glandulosa, S. guianensis), or only small appendages (Blastemanthus) may exist (Amaral, 1991). The outer appendages are best interpreted as a corona in colors that contrast with the real staminodes. However, these have also been described as staminodes (e.g., Amaral, 1991). The same interpretation holds for the corona of the Passifloraceae (Table III).

4. In the asterids, several families have "scales" on the corolla alternating with the stamens (e.g., in Apocynaceae, Boraginaceae, Cuscutaceae, Menyanthaceae, Hydrophyllaceae). These have occasionally been interpreted as stipular (e.g., Woodson & Moore, 1938) or staminodial in nature (Lindley, 1853, cited in Lawrence, 1937). However, other floral anatomical studies have shown that the scales are invaginations of the corolla tube, wit no relation to the androecium (e.g., Eichler, 1875-1 878; Lawrence, 1937; Rao & Arati Ganguli, 1963).

5. Intrastaminal appendages or lobes functioning as nectary have often been interpreted as evidence of staminodes or even carpellodes in the asterids, especially when the external morphology is reminiscent of these (Figs. 48-51; Eichler, 1875-1878; Sersic & Cocucci, 1999; Woodson & Moore, 1938). Other examples of incongruent interpretations are given in Table III.

B. RECEPTACULAR DISKS

Disklike nectaries (Figs. 42-47) also belong to the category of imaginary staminodes because they have often been taken for an aborted whorl of stamens (see Table III). This is illustrated by following examples;

1. In the Rhamnaceae there is no external (ontogenetic) evidence of a second staminodial whorl (Fig. 45); nor is there any link between androecium and disk (Bennek, 1958; Suessenguth, 1953a). However, the vascular supply of the disk, which can sometimes be similar to that of the antepetalous stamens, along with the disruption of the "alternance rule" (the stamens are antepetalous), has been used as support for the interpretation of the intrastaminal disk as modified stamens (Nair & Sarma, 1961; Prichard, 1955). Both interpretations--that is, the ontogenetic and the anatomical--can be supported to some extent, as another stamen whorl may have been present in an ancestral state but may be lost in extant Rhamnaceae. This interpretation is also linked to what family is considered the nearest sister group. The development of a disk can have "taken up" the vascular facilities provided for the now-missing antesepalous stamens. This demonstrates that a total rejection of the idea of a "lost" whorl, as well as the rec ognition of "evidence" of a lost whorl, are not to be considered too strictly. The derivation of an (ob)haplostemonous androecium from two stamen whorls could be described as a counterbalancing development within the flower, because the space occupied by stamens is invariably taken over by the developing disk. However, we occasionally observed an antesepalous staminode in Zizyphus lotus (Ronse Decraene, unpubl.), which does not support the interpretation of a staminodial disk.

2. In the Polygonaceae the position of lost stamens is often taken over by receptacular nectaries (Figs. 42-43). Emberger (1939) interpreted the nectaries of Fagopyrum as staminodes, because of the spatial and numerical correlation between stamens and nectaries. Indeed, there is a high correlation between the number of stamens and the presence of the glands. However, the internal variations of nectarial tissue, as well as anatomical evidence, firmly deny a staminodial nature (cf. Ronse Decraene & Akeroyd, 1988; Ronse Decraene & Smets, 1991c).

More examples of incongruent disks are given in Table III.

C. THE CONTEXT OF IMAGINATIVE THOUGHT

Interpretations of the homology of disk structures have varied according to the methods of investigation used. Floral anatomists attached greater importance to vascular elements and more often favored a phyllomatic (staminodial) nature; therefore, they interpreted floral disks more likely as transformed (reduced) organs. Scholars in floral ontogeny and systematists often ignored the vasculature and favored an interpretation of a receptacular nature for the disk, because of its late inception and the absence of a clear morphological resemblance to other floral organs. This has often resulted in contradictory interpretations in floral morphology. However, it is essential that both methods of investigations be given sufficient weight (see Arber, 1933; Gustafsson & Albert, 1999).

Floral anatomists, especially the American school of Eames (e.g., Berkeley, 1953; Blaser, 1954; Dawson, 1936; Eames, 1931, 1961; Heinig, 1951; Prichard, 1955; Tillson & Bamford, 1938) and the Indian school of Puri (e.g., Nair & Jain, 1956; Nair & Joshi, 1958; Nair & Sarma, 1961; Narayana & Rao, 1971; Puri, 1948) have been obsessive about describing staminodial structures on the basis of the presence of vascular traces and the current belief of primitive polyandry in angiosperms. Indeed, interpretations of staminodial structures (especially for disks) were often related with a hypothetical interpretation of ancestral polyandry and a given direction of evolution (e.g., Humiriaceae: Narayana & Rao, 1978; Geraniaceae: Dawson, 1936). This led to certain highly imaginative reconstructions of "ancestral" flowers.

Evidence of a staminodial nature of the disk was often sought in the presence of vestigial vascular stubs or vascular connections between the supply to the stamens or other organs and the disk (e.g., Nair & Joshi, 1958). There are indefinite possibilities for supplying the disk; the supply of the nectary is opportunistic as it becomes derived from the nearest source of vascular tissue, which is often the androecium. Trying to recognize staminodes or any other structures surrounding the ovary, if no structural evidence of their homology with stamens exists, is senseless. Smets (1986, 1988a, 1988b) restricted the term "disk nectary" to a secondary emergence of the receptacle (nectaria axialia) when there is no homology possible with staminodes and when it is not part of the gynoecium.

VI. Molecular Developmental Genetics and Staminodes

Recently, much emphasis has been laid on the study of expression of developmental genes in order to understand differences of morphological characters from an ontogenetic and phylogenetic perspective. Studies of the molecular controlling mechanisms of organ determination have led to the discovery of MADS box genes (see, e.g., Albert et al., 1998; Thei[beta]en et al., 1996; Yanofsky, 1995). These genes are partly responsible for floral organ determination, as demonstrated in the ABC model, with three distinct functions (Coen, 1991; Coen & Meyerowitz, 1991). In its simplest form the ABC model implies that A is responsible for sepal expression, A + B for petals, B + C for stamens, and C for carpels. Beyond the expression of this simple model, the overall expression of flower development is often more complex (see Albert et al., 1998; Kramer & Irish, 2000). Two gene activities have to be recognized, leading to a distinction between whorl identity and organ identity: one that influences the outcome or function of an organ (whether it be sepaloid or petaloid, etc.), or process orthology; and one that influences the position of organs, or positional orthology.

These two processes act independently, as a petaloid organ will occupy the same position as the original organ. For example, in double-flowered Begonia (Lehmann & Sattler, 1989; Ronse Decraene & Smets, 1990b), stamens have been replaced by petaloid structures that occupy the same position in the flower. On the other hand, in Macleaya stamens occur in the position of the petals in the other Papaveraceae (Ronse Decraene & Smets, 1990b) and in Calla (Araceae) in the position of tepals (Lehmann & Sattler, 1992).

Albert et al. (1998) interpreted the nature of organs mainly on the basis of gene activity. In a simple way AB gives petals, BC stamens, and ABC leads to staminodes. Staminodes thus appear as the result of an overlap of the genetic programs of the perianth members and stamens during floral development (cf. Erbar et al. [1998] for the nectar leaves of Ranunculaceae).

Through examples of Lecythidaceae and Clusiaceae, Albert et al. (1998) and Gustafsson (2000) correlated the formation of staminodial structures with the expansion of the A function gene activity, which leads to the transference of petaloid characters to stamens.

However, this approach has certain shortcomings. The terminological distinction in zones of influence is not sufficiently detailed to recognize intrinsic variations of expressions of organs (there are different degrees of staminode development), it overlooks external environmental factors and pressures from pollinators, and it denies the historical dimension (what is derived from what), as process homology is equally influenced by time.

The explanation of a shift in gene activity is only a partial explanation for the existence of staminodes, as it is mainly a functional (teleological) explanation of gene activity. In the case of the nectar leaves of Ranunculaceae, Erbar et al. (1998) have demonstrated the homology with stamens in the presence of rudimentary adaxial pollen sacs in early developmental stages. The shift to an increasing A function may have been progressive or sudden, but little can be said about that, as the knowledge of the importance of genetic mutations to evolution is virtually nil.

A good case for the oversimplification of the molecular model is the example of sorrel or Rumex (Polygonaceae). In Rumex the perianth consists of two whorls of three sepaloid tepals. Ainsworth et al. (1995) and Albert et al. (1998) hypothesized that petals were ancestrally present in Rumex but that they were lost in evolution. They explain the present sepaloid perianth as the result of the loss of the B function and thus as the result of a secondary restriction of the "basal" petaloidy that is considered ancestral in the family. This explanation does not account for the shifts between trimery and pentamery operating in the family, the occurrence of outer stamen pairs, and the improbable distinction between petals and sepals that may not have been present in the ancestors of the Polygonaceae, as no extant Polygonaceae with both sepals and petals exist. The molecular explanation may refer to the process of development, but it is only partial evidence, as the hypothesized assumptions about the evolution of petal s have no morphological basis.

To restrict the explanation for stamen, staminode, and petal identity to an alteration in expression or function of B-class genes (e.g., Albert et al., 1998; Bowman et al., 1991; Weigel & Meyerowitz, 1994) is to oversimplify the development and identity of organs. The distinctions made between bracteopetals and andropetals by Hiepko (1965) and Takhtajan (1991), or the terms "homeosis"or "heterotopy," as the total or partial replacement of one part by another of the same organism (e.g., Sattler, 1988, 1994; Li & Johnston, 2000) explain the same as the molecular terminology, but they are based on a different point of view.

VII. Concluding Remarks

It is clear that the decision to recognize a lately arising primordium as a staminodium or merely as a secondary receptacular emergence is often a matter of subjective appreciation and is extremely difficult to assess. Therefore, reliance on indirect evidence can be helpful. For Harungana (Clusiaceae), Ronse Decraene and Smets (199la) hypothesized that the nectaries represent a staminodial whorl, and evidence was given in the vasculature and the external shape. In Proteaceae, Douglas and Tucker (1996) refuted a staminodial nature for the intervening nectary scales, although these are strictly speaking comparable to the nectary scales of the Clusiaceae. Proposed phylogenetic relationships (e.g., Chase et al., 1993; APG, 1998) can help in assigning the true nature of organs, although this evidence could be subject to circular reasoning. The association of Clusiaceae with clades having diplostemonous flowers (e.g., Linales, Ochnaceae, rosids I) supports the acceptance of a staminodial nature of the nectaries in Harungana. The association of Proteaceae with the Platanaceac at the base of the eudicots may be evidence against a staminodial nature.

Staminodial structures play an important role in floral evolution (see also Walker-Larsen & Harder, 2000). They are a reflection of the dynamism of the androecium (and flower) in response to changing conditions. Therefore, their importance should not be ignored, and a misinterpretation of structures that resemble staminodes must be recognized. The recognition of types of staminodial structures based on function (i.e., vestigial and functional staminodes) and position is only a partial characterization, but it is a necessary reflection of the complexity of floral forms.

VIII. Acknowledgments

We acknowledge the technical assistance of Anja Vandeperre in preparing the photographic material. This research was supported by a grant from the Research Council of the Katholieke Universiteit Leuven (0T/97/23).

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Weigel, D. & E. M. Meyerowitz. 1994. The ABCs of floral homeotic genes. Cell 78: 203-209.

Winkler H. 1931. Linaceae. Pp. 82-130 in A. Engler & K. Prantl (eds.), Die naturlichen Pflanzenfamilien. Ed. 2. Vol. 19a. Engelmann, Leipzig.

Woodson, R. E. & J. A. Moore. 1938. The vascular anatomy and comparative morphology of Apocynaceous flowers. Bull. Torrey Bot. Club 65: 135-165.

Woon, C. & H. Keng. 1979. Stamens of the Dipterocarpaceae. Gard. Bull., Singapore 32: 1-51.

Worsdell, W. C. 1903. The origin of the perianth of flowers with special reference to the Ranunculaceae. New Phytol. 2: 42-48.

Wydler, H. 1863. Ueber die Bluthe von Melianthus. Flora 1863: 145-151.

Yanofsky, M. F. 1995. Floral meristems to floral organs: Genes controlling early events in Arabidopsis flower development. Annual Rev. Pl. Physiol. Pl. Molec. Biol. 46: 167-188.

Zohary, M. & B. Baum. 1965. On the androecium of Tamarix flower and its evolutionary trends. Israel J. Bot. 14: 101-111.
Table I

The occurrence of complete staminodial whorls in the Magnoliatae as
derived from (ob)diplostemonous or dicyclic androccia (a)



Family              Tribe, genus, or species

Alliaceae           Allium, Trichlora, Gilliesia
Anacardiaceae       Pentaspadon
Bombacaceae         Chorisia
Bonnetiaceae        Ploiarium, Archytaea

Brexiaceae          Brexia, Ixerba
Burseraceae         Santiria
Caesalpiniaceae     Dimorphandra
Caryophyllaceae     Paronychia, Herniaria,
                      Habrosia, Schiedea, etc.


Celastraceae        Lophopyxis
 (Lophopyxidaceae)
Combretaceae        Thiloa
Commelinaceae       Murdania, Anthericopsis
                      (1), Palisota (2)
Connaraceae         Connarus
Corynocarpaceae     Corynocarpus


Crassulaceae        Sempervivum
Diapensiaceae       All
Dioscoreaceae       Dioscorea sects. Macrocarpaea
                      Asterotricha
Dipterocarpaceae    Dipterocarpus oblongifolius
Fabaceae            Teramnus, Biserrula sp.,
                      Vicia sp., etc.

Geraniaceae         Erodium

Hamamelidaceae (b)  Hamamelis, Corylopsis,
                      Loropetalum,

Hyacinthaceae       Albuca
Hydnoraceae         Prosopanche
Hydrocharitaceae    Lagarosiphon
Johnsoniaceae       Hodgsoniola
Lepuropetalaceae    Lepuropetalon
Loasaceae           Mentzelia sect. Bartonia
Lomandraceae        Sowerbaea
Linaceae            Linum, Reinwardtia, etc.



Medusandraceae      Medusandra
Melastomataceae     Poteranthera, Anplectrum
Meliaceae           Toona, Cedrela

Mimosaceae          Pentaclethra
Moringaceae         Moringa

Myrsinaceae         Myrsine
Myrtaceae           Darwinia, Chamaelaucium

Ochnaceae           Sauvagesia, Leitgebia
Olacaceae           Olax (c), Liriosma

Onagraceae          Clarkia sp.
Oxalidaceae         Averrhoa, Oxalis corniculata


Parnassiaceae       Parnassia

Primulaceae         Samolus

Pterostemonaceae    Pterostemon
Ranunculaceae       Clematis sect. Atragene
Rutaceae            Diosmeae, Flindersia

Sapotaceae          Magodendron, Mimusops, Synsepalum,
                      Achras, etc.

Simaroubaceae       Alvaradoa
Sterculiaceae       Buettneria, Theobroma, Abroma, etc.

Suriancaceae        Suriana
Themidaceae         Brodiaea, Dichelostemma
Theophrastaceae     All
Thymelaeaceae       Gnidia, Craspedostoma
Tiliaceae           Brownlowia, Pentace

Triuridaceae        Seychellaria

Xyridaceae          Xyris
Zygophyllaceae      Tribulus (occasionally)

                    Position of
                    staminodial
Family              whorl

Alliaceae           Opposite inner tepals
Anacardiaceae       Antepetalous
Bombacaceae         Antesepalous
Bonnetiaceae        Antepetalous

Brexiaceae          Antepetalous
Burseraceae         Antepetalous
Caesalpiniaceae     Antesepalous
Caryophyllaceae     Antepetalous



Celastraceae        Antepetalous
 (Lophopyxidaceae)
Combretaceae        Antepetalous
Commelinaceae       Opposite inner (1) or
                      outer tepals (2)
Connaraceae         Antepetalous
Corynocarpaceae     Antesepalous


Crassulaceae        Antepetalous
Diapensiaceae       Antepetalous
Dioscoreaceae       Opposite inner tepals

Dipterocarpaceae    Antesepalous
Fabaceae            Antepetalous


Geraniaceae         Antepetalous

Hamamelidaceae (b)  Antepetalous


Hyacinthaceae       Opposite outer tepals
Hydnoraceae         Alternitepalous
Hydrocharitaceae    Opposite outer tepals
Johnsoniaceae       Opposite outer tepals
Lepuropetalaceae    Antepetalous
Loasaceae           Antesepalous
Lomandraceae        Opposite outer tepals
Linaceae            Antepetalous



Medusandraceae      Antesepalous
Melastomataceae     Antepetalous
Meliaceae           Antepetalous

Mimosaceae          Antepetalous
Moringaceae         Antesepalous

Myrsinaceae         Antesepalous
Myrtaceae           Antepetalous

Ochnaceae           Antepetalous
Olacaceae           Antepetalous

Onagraceae          Antepetalous
Oxalidaceae         Antepetalous


Parnassiaceae       Antepetalous

Primulaceae         Antesepalous

Pterostemonaceae    Antepetalous
Ranunculaceae       Alternitepalous
Rutaceae            Antepetalous

Sapotaceae          Antesepalous


Simaroubaceae       Antepetalous
Sterculiaceae       Antesepalous,

Suriancaceae        Antepetalous
Themidaceae         Opposite outer tepals
Theophrastaceae     Antesepalous
Thymelaeaceae       Antesepalous
Tiliaceae           Antepetalous

Triuridaceae        Opposite inner tepals

Xyridaceae          Opposite outer tepals
Zygophyllaceae      Antesepalous



Family              Authority

Alliaceae           Rahn, 1998
Anacardiaceae       Eichler, 1878
Bombacaceae         Eichler, 1878
Bonnetiaceae        Dickison & Weitzman,
                      1998
Brexiaceae          Bensel & Palser, 1975a
Burseraceae         Engler, 1931d
Caesalpiniaceae     Eichler, 1878
Caryophyllaceae     Ronse Decraene et al.,
                      1998b; Wagner &
                      Harris, 2000; Figs.
                      17-18
Celastraceae        Cronquist, 1981
 (Lophopyxidaceae)
Combretaceae        Eichler, 1878
Commelinaceae       Faden, 1998

Connaraceae         Saunders, 1939
Corynocarpaceae     Narayana et al., 1986;
                      Philipson, 1987;
                      Figs. 7-8
Crassulaceae        Berger, 1930
Diapensiaceae       Palser, 1962
Dioscoreaceae       Huber, 1998

Dipterocarpaceae    Woon & Keng, 1979
Fabaceae            Eichler, 1878;
                      Rodriguez-Riano
                      et al., 1999
Geraniaceae         Kumar, 1976; Payer,
                      1857; Figs. 12-13
Hamamelidaceae (b)  Endress, 1967; Mione
                      & Bogle, 1990; Figs.
                      15-16
Hyacinthaceae       Speta, 1998
Hydnoraceae         Cocucci, 1975
Hydrocharitaceae    Cook, 1998
Johnsoniaceae       Clifford & Conran, 1998
Lepuropetalaceae    Engler, 1930b
Loasaceae           Urban, 1892
Lomandraceae        Conran, 1998
Linaceae            Kumar, 1976; Narayana,
                      1964; Narayana &
                      Rao 1971, 1976a,
                      1976b, 1977a, 1977b
Medusandraceae      Cronquist, 1981
Melastomataceae     Eichler, 1878
Meliaceae           Harms, 1960, Sheela
                      Lal, 1994
Mimosaceae          Eichler, 1878
Moringaceae         Ronse Decraene et al., 1998a;
                     Figs. 1-2
Myrsinaceae         Caris, 1998
Myrtaceae           Baillon, 1873; Ronse Decraene &
                     Smets, 1991b
Ochnaceae           Eichler, 1878; Goebel, 1933
Olacaceae           Agarwal, 1963; Baillon, 1892;
                     Sleumer, 1935
Onagraceae          Eichler, 1878
Oxalidaceae         Al-Nowaihi & Khalifa, 1971;
                     Eichler, 1878; Kumar, 1976;
                     Moncur, 1988; Fig. 14
Parnassiaceae       Bensel & Palser, 1975a; Engler,
                     1930b; Saxena, 1976
Primulaceae         Caris, 1998; Ronse Decraene &
                     Smets, 1995a; Sattler, 1962
Pterostemonaceae    Engler, 1930b
Ranunculaceae       Eichler, 1878
Rutaceae            Engler, 1931b; Sheela Lal &
                     Narayana, 1994
Sapotaceae          Ayensu, 1972; Eichler, 1878;
                     Hartog, 1878, Moncur, 1988;
                     Pennington, 1991; Vink, 1995
Simaroubaceae       Engler, 1931c
Sterculiaceae       Venkata Rao, 1952; Heel, 1966; Fig.
                     38
Suriancaceae        Tschunko & Nickerson, 1976
Themidaceae         Rahn, 1998
Theophrastaceae     Cronquist, 1981; Eichler, 1878
Thymelaeaceae       Domke, 1934; Gilg, 1894
Tiliaceae           Bocquillon, 1866; Eichler, 1878;
                     Heel, 1966
Triuridaceae        Maas-van de Kamer & Weustenfeld,
                     1998
Xyridaceae          Kral, 1998
Zygophyllaceae      Engler, 1931a

(a)No information is available for Centroplacus (Pandaceae),
Daphniphyllaceae.

(b)The nectaries of Hamamelis represent an inner staminodial whorl,
whereas in Corylopsis one or two whorls of supplementary staminodial
nectaries are said to arise next to the staminodial whorl (Endress,
1967). We observed that an antepetalous staminodial whorl is initiated
following antesepalous stamen initiation before gynoecium initiation.
Two inner protuberances bearing stomata are initiated much later and
represent--we believe--receptacular nectaries (Figs. 15-16).

(c)Not exactly antepetalous in Olax due to reductions of stamen number.
Table II

Presence of staminodes within a whorl of fertile stamens

Key: 1 = antesepalous whorl; 2 = antepetalous whorl (alternisepalous
whorl); 3 = antesepalous and atenpetalous whorl; 4 = position of
staminodes; 5 = number of staminodes; 6 = presence of zygomorphy in the
flower

Family                               Genus

Anacardiaceae (Figs. 20-21)          Mangifera, Anacardium
Amaranthaceae                        Lithosperma
Bignoniaceae                         Catalpa, Kigelia
Caesalpiniaceae                      Tamarindus, Bauhinia, Cassia,
                                       Amherstia, etc.
Cannaceae                            Canna
Capparaceae (Figs. 4-6)              Euadenia, Dactylaena

Caryophyllaceae                      Microphyes (1), Ortegia (2)
Chrysobalanaceae                     Hirtella, Parinarium
Combretaceae                         Lumnitzera

Commelinaceae                        Cochliostema (1) Palisota (2),
                                       Murdannia (3), Polyspatha etc.
                                       (4)
Costaceae                            All


Dichapetalaceae                      Tapura
Gentianaceae                         Hoppea
Geraniaceae                          Pelargonium
Gesneriaceae                         Sanango
Globulariaceae (incl. Selaginaceae)  Globularia
Haemodoraceae                        Schiekia (1), Pyrrorhiza (2)
Heliconiaceae                        Heliconia
Hydrocharitaceae                     Nechamandra, Maidenia,
                                       Vallisneria

Krameriaceae                         Krameria
Lamiaceae (a)                        Lavendula, Bystropogon, Salvia
Linnacaceae                          Linnaea, Abelia
Loasaceae                            Petalonyx crenatus
Loganiaceae                          Usteria guineensis
Malpighiaceae                        Stigmaphyllon, Gaudichaudia,
                                       Camarea
Marantaceae                          All

Mimosaceae                           Neptunia (Staminate flowers)
Morinaceae                           Morina
Musaceae                             Musa
Myoporaceae                          Oftia, etc.
Olacaceae                            Ptychopetalum
Onagraceae                           Lopezia
Orchidaceae                          All
Pedaliaceae (incl.                   Martynia, Sesamen
  Martyniaceae,
  Trapellaceae)
Podostemonaceae                      Podostemon
Pontederiaceae                       Hydrothrix
Proteaceae                           Conospermum, Protea (1),
                                       Synaphea (2), Placospermum (3)

Rutaceae                             Cusparieae

Sabiaceae                            Meliosma
Solanaceae                           Salpiglossis, Schizanthus,
                                       Anthocercis
Scrophulariaceae                     Bonnaya, Gratiola (1), Ixianthus
                                       (2), Digitalis (3), etc.

Surianaceae                          Suriana

Tecophyllaeaceae                     Tecophilaea (1), Zephyra (2)
Trigoniaceae                         Trigonia (1), Lightia (2)


Verbenaceae                          Duranta, Stachytarpheta, Lantana,
                                       etc.
Vochysiaceae                         Salvertia, Vochysia, Qualea

Zingiberaceae                        All

Family                               1  2  3

Anacardiaceae (Figs. 20-21)          -  -  +
Amaranthaceae                        +  -  -
Bignoniaceae                         +  -  -
Caesalpiniaceae                      +  +  -

Cannaceae                            -  -  +
Capparaceae (Figs. 4-6)              +  -  -

Caryophyllaceae                      +  -  -
Chrysobalanaceae                     -  -  +
Combretaceae                         -  +  -

Commelinaceae                        +  +  +


Costaceae                            -  -  +


Dichapetalaceae                      +  -  -
Gentianaceae                         +  -  -
Geraniaceae                          -  +  -
Gesneriaceae                         +  -  -
Globulariaceae (incl. Selaginaceae)  +  -  -
Haemodoraceae                        +  +  -
Heliconiaceae                        +  -  -
Hydrocharitaceae                     -  +  +


Krameriaceae                         +  -  -
Lamiaceae (a)                        +  -  -
Linnacaceae                          +  -  -
Loasaceae                            1  -  -
Loganiaceae                          +  -  -
Malpighiaceae                        +  -  -

Marantaceae                          -  -  +

Mimosaceae                           -  -  +
Morinaceae                           +  -  -
Musaceae                             -  +  -
Myoporaceae                          +  -  -
Olacaceae                            +  -  -
Onagraceae                           +  -  -
Orchidaceae                          +  +  -
Pedaliaceae (incl.                   +  -  -
  Martyniaceae,
  Trapellaceae)
Podostemonaceae                      -  -  -
Pontederiaceae                       +  -  -
Proteaceae                           +  -  -


Rutaceae                             +  -  +

Sabiaceae                            -  +  -
Solanaceae                           +  -  -

Scrophulariaceae                     +  -  -


Surianaceae                          -  +  -

Tecophyllaeaceae                     +  -  +
Trigoniaceae                         +  -  +


Verbenaceae                          +  -  -

Vochysiaceae                         -  +  -

Zingiberaceae                        -  -  +

Family                               4

Anacardiaceae (Figs. 20-21)          One antesepalous fertile
Amaranthaceae                        ?
Bignoniaceae                         Adaxial upper, or three adaxial
Caesalpiniaceae                      S2, 5/P post, Spost+P

Cannaceae                            Only Ppost fertile
Capparaceae (Figs. 4-6)              Slat & Spost

Caryophyllaceae                      S1, S2 (1), S4, S5 (2)
Chrysobalanaceae                     Spost Ppost
Combretaceae                         Antepetalous (variable number of
                                       stamens)
Commelinaceae                        Pant+Sant-lat (1), Plat-post (2),
                                       Spost (3), Plat-post+Spost (4)

Costaceae                            S, Plat-post?


Dichapetalaceae                      S2,S4
Gentianaceae                         ?
Geraniaceae                          Pant
Gesneriaceae                         Spost
Globulariaceae (incl. Selaginaceae)  Spost (vascular bundle)
Haemodoraceae                        Slat-ant (1) or Plat-post (2)
Heliconiaceae                        Sant
Hydrocharitaceae                     Alternitepalous (and antetepalous
                                       if petal considered as staminode)

Krameriaceae                         Sant (S1)
Lamiaceae (a)                        Spost, S4 and S5 (Slat-post)
Linnacaceae                          S2
Loasaceae                            Spost and Slat-post
Loganiaceae                          Spost (fertile or absent)
Malpighiaceae                        S1, 5

Marantaceae                          Plat-ant or 0, Slat-post (only
                                       Ppost fertile)
Mimosaceae                           Abaxial stamens
Morinaceae                           Slat-ant (S1,S3?)
Musaceae                             Ppost
Myoporaceae                          Spost
Olacaceae                            Alternipetalous
Onagraceae                           Sant
Orchidaceae                          Spost, Plat-post
Pedaliaceae (incl.                   Spost, Slat-ant
  Martyniaceae,
  Trapellaceae)
Podostemonaceae                      Incomplete inner whorl
Pontederiaceae                       ?
Proteaceae                           Sab (1), Sad (2), Slat and Sab (3)


Rutaceae                             S2, 3, 5(4), Ppost

Sabiaceae                            Opp. Pant and Ppost
Solanaceae                           Sant (opp. sepal 1), S1,2,5

Scrophulariaceae                     Slat-ant (1), Slat-post (2),
                                       Spost (3)

Surianaceae                          Antepetalous, variable (combination
                                       of fertile and sterile stamens
Tecophyllaeaceae                     Ppost+Slat-post (1), Slat-post (2)
Trigoniaceae                         In adaxial part of flower (1), S3
                                       (2), partly transformed as stami-
                                        nodes
Verbenaceae                          Sab, Slat-ant

Vochysiaceae                         Plat & ant

Zingiberaceae                        Plat-ant, Slat-post

Family                                        5           6

Anacardiaceae (Figs. 20-21)                   9           +
Amaranthaceae                                 3           -
Bignoniaceae                                1, 3          +
Caesalpiniaceae                            1-2, 6         +

Cannaceae                                 1-4 (-5)        +
Capparaceae (Figs. 4-6)                       3           +

Caryophyllaceae                               2           -
Chrysobalanaceae                              ?           +
Combretaceae                                  1           +

Commelinaceae                              1, 2-3         +


Costaceae                                 5, fused        +
                                            into
                                          labellum
Dichapetalaceae                               2           +
Gentianaceae                                 2-3          ?
Geraniaceae                                   3           +
Gesneriaceae                             1 or absent      +
Globulariaceae (incl. Selaginaceae)           1           +
Haemodoraceae                                 2           +
Heliconiaceae                                 1           +
Hydrocharitaceae                          1-2? (if        +
                                     petal considered as
                                         staminode)
Krameriaceae                                  1           +
Lamiaceae (a)                                1-2          +
Linnacaceae                                   1           +
Loasaceae                                     3           -
Loganiaceae                                   1           +
Malpighiaceae                                2-3          +

Marantaceae                               1-2(0)+2        +

Mimosaceae                                    3           +
Morinaceae                                    2           +
Musaceae                                      1           +
Myoporaceae                              1 or absent      +
Olacaceae                                     3           -
Onagraceae                                    1           +
Orchidaceae                                 1, 2          +
Pedaliaceae (incl.                          1, 2          +
  Martyniaceae,
  Trapellaceae)
Podostemonaceae                               1           -
Pontederiaceae                                2           -
Proteaceae                                    1           +


Rutaceae                                     3-5          +

Sabiaceae                                     3           -
Solanaceae                                  1, 3          +

Scrophulariaceae                             1,2          +


Surianaceae                                  1-5          -

Tecophyllaeaceae                             2-3          +
Trigoniaceae                              2-6 (1),        +
                                            1 (2)

Verbenaceae                                1, 2, 3        +

Vochysiaceae                                2, 4          +

Zingiberaceae                                2+2          +

Family                               Authority

Anacardiaceae (Figs. 20-21)          Copeland, 1961; Sharma, 1954
Amaranthaceae                        Eliasson, 1988
Bignoniaceae                         Eichler, 1875; Neubauer, 1959
Caesalpiniaceae                      Eichler, 1878; Tucker, 1988b,
                                       1988c, 1996, 1997, 1998
Cannaceae                            Kress, 1990
Capparaceae (Figs. 4-6)              Karrer, 1991; Pax & Hoffmann,
                                       1936; Ronse Decraene, unpubl.
Caryophyllaceae                      Ronse Decraene et al., 1998b
Chrysobalanaceae                     Eichler, 1878
Combretaceae                         Fukuoka et al., 1998

Commelinaceae                        Faden, 1998


Costaceae                            Larsen, 1998


Dichapetalaceae                      Baillon, 1874
Gentianaceae                         Kshetrapal, 1973
Geraniaceae                          Kumar, 1976; Sattler, 1973
Gesneriaceae                         Dickison, 1994
Globulariaceae (incl. Selaginaceae)  Saunders, 1937
Haemodoraceae                        Simpson, 1998
Heliconiaceae                        Andersson, 1998
Hydrocharitaceae                     Cook, 1998; McConchie &
                                       Kadereit, 1987

Krameriaceae                         Cronquist, 1981
Lamiaceae (a)                        Eichler, 1875; Payer 1857
Linnacaceae                          Eichler, 1875
Loasaceae                            Urban, 1892
Loganiaceae                          Hakki, 1998
Malpighiaceae                        Eichler, 1878

Marantaceae                          Anderson, 1998; Eichler, 1878;
                                       Kress, 1990
Mimosaceae                           Tucker, 1988a
Morinaceae                           Hofmann & Gottmann, 1990
Musaceae                             Kress, 1990
Myoporaceae                          Bocquillon, 1861a; Cronquist, 1981
Olacaceae                            Sleumer, 1935: fig. 1H
Onagraceae                           Eyde & Morgan, 1973
Orchidaceae                          Endress, 1994
Pedaliaceae (incl.                   Baillon, 1861, 1862c; Cronquist,
  Martyniaceae,                        1981
  Trapellaceae)
Podostemonaceae                      Baillon, 1886; Rutishauser, 1997
Pontederiaceae                       Cook, 1998
Proteaceae                           Haber, 1959, 1966; Douglas, 1997
                                       (1,2); Douglas & Tucker, 1996
                                       (3)
Rutaceae                             Baillon, 1872; Eichler, 1878;
                                       Kallunki, 1998
Sabiaceae                            Beusckom, 1971
Solanaceae                           Eichler, 1875; Mair, 1977; Murray,
                                       1945
Scrophulariaceae                     Chatin, 1873a; Eichler, 1875;
                                       Payer, 1857; Singh, 1979; Walker-
                                       Larsen & Harder, 2000
Surianaceae                          Gutzwiller, 1961; Tschunko &
                                       Nickerson, 1976
Tecophyllaeaceae                     Simpson & Rudall, 1998
Trigoniaceae                         Eichler, 1878; Kopka & Weberling,
                                       1983; Smets, 1988a

Verbenaceae                          Bocquillon, 1861b; Eichler, 1875;
                                       Payer, 1857; Sattler, 1973
Vochysiaceae                         Eichler, 1878; Kopka & Weberling,
                                       1983; Litt, 1997
Zingiberaceae                        Larsen et al., 1998

(a)Payer (1857) described the initiation and later abortion of the
posterior staminode in the Lamiaceae. This is rejected by Chatin
(1873a), who states that no trace of a fifth stamen exists in the
Labiates, unlike the Scrophulariaceae. Eichler (1875) mentions the
presence of a rudimentary stamen in Bystropogan.
Table III

Various misinterpretations of receptacular emergences as staminodes
(pseudostamiondes), carpellodes, or structures with unknown or debatable
homologies


Family                         Genus or species

Achariaceae                    Ceratiosicyos, Acharia,
                                 Guthriea

Aextoxicaceae                  Aextoxicon


Amaranthaceae                  Achyranthes, etc.




Apocybaceae (Figs. 48-49)      Vinca, Allamanda, etc.



Bataceac                       Batis






Brassicaceae                   None



Burseraceae                    Balsamodendron

Capparaceae                    Cadaba, Capparis



Celastraceae                   Celastrus


Clusiaceae                     Hypericum, Harungana,
                                 etc.

Crassulaceae                   None


Ctenolophaceae                 Ctenolophon

Dichapetalaceae (Figs. 26-28)  Dichapetalum


Dipentodonta-                  Dipentodon
  ceae
Epacridaceae                   None






Euphorbiaceae                  Croton, Cluytia,
                                 Mercurialis,
                                 etc.







Fabaceae                       Phascoleae



Flacourtiaceae                 Casearia, Azara,
  (Figs. 36-                     etc.
  37, 39-40)




Francoaceae                    Francoa



Geraniaceae                    Geranium, Pelar-
                                 gonium



Greyiaceae (Figs. 10-11)       Greyia

Humiriaccae                    Sacoglottis, Vantanea, Humiria,
                                 etc.





Hydrophyllaceae                Phacelia glaberrima


Ixonanthaceae                  Ixonanthes, Ochthocosmus
Lauraceae                      None
  (Fig. 41)







Lepidobotrya-                  Lepidobotrys
  ceae
Melianthaceae                  Melianthus








Nyctaginaceae                  Mirabilis



Ochnaceae                      Sauvagesia






Olacaceae (b)                  Aptandra, Strom-
                                 bosia, Octok-
                                 nema, etc.
Opiliaceae                     Opilia







Oxalidaceae                    Oxalis



Paeoniaceae                    Paeonia





Passifloraceae (c)             Passiflora, Adenia,
                                 Crossostema, etc.










Peridiscaceae                  Peridiscus

Podostemonaceae                Polypleurum, etc.


Polemoniaceae                  Cantua, Cobaea, Phlox
  (Fig. 47)


Polygonaceae                   Fagopyrum, Polygonum
  (Figs. 42-43)

Primulaceae                    Primula, Soldanella





Proteacceae                    None

Rhamnaceae                     Zizyphus, Helinus, etc.
  (Fig. 45)


Rhizophoraceae                 Crossostylis


Rubiaceae                      Mitchella





Rutaceae                       None





Salvadoraceae                  Salvadora, Dobera





Sapindaceae                    Xanthoceras


Sarcolaenaceae                 Xyloolaena






Scyphostegiaceae               Scyphostegia






Simaroubaceac                  Picrasma, Brucea
                                 (1); Samadera
                                 (2); Picramnw,
                                 Eurycoma, etc.



Stackhousiaceae                Stackhousia,
                                 Tripterococcus



Tamaricaceae                   Tamarix





Thymelaeaceac                  None



Turneracceae                   Turnera, etc.



Vitaceac (including Leeaceae)  Leca, Vitis
  (Fig. 44)


Zygophyllaceae                 Balanites




                               Protagonist
Family                         evidence

Achariaceae                    External


Aextoxicaceae                  External


Amaranthaceae                  External




Apocybaceae (Figs. 48-49)      Anatomical link with the
                                 gynoecium


Bataceac                       External, no anatomical






Brassicaceae                   External



Burseraceae                    Anatomical

Capparaceae                    Anatomical, external



Celastraceae                   Anatomical


Clusiaceae                     Anatomical, ontogenetic


Crassulaceae                   External, anatomical


Ctenolophaceae                 Anatomical

Dichapetalaceae (Figs. 26-28)  External


Dipentodonta-                  External
  ceae
Epacridaceae                   External






Euphorbiaceae                  External









Fabaceae                       Anatomical



Flacourtiaceae                 External
  (Figs. 36-
  37, 39-40)




Francoaceae                    External



Geraniaceae                    Anatomical




Greyiaceae (Figs. 10-11)       External

Humiriaccae                    External






Hydrophyllaceae                External


Ixonanthaceae                  Anatomical
Lauraceae                      Anatomical, external
  (Fig. 41)







Lepidobotrya-                  Anatomical
  ceae
Melianthaceae                  External








Nyctaginaceae                  External



Ochnaceae                      External, ana-
                                 tomical





Olacaceae (b)                  External


Opiliaceae                     External







Oxalidaceae                    External, anatomical



Paeoniaceae                    Anatomical





Passifloraceae (c)             External, anatomical,
                                 developmental










Peridiscaceae                  External

Podostemonaceae                External


Polemoniaceae                  Anatomical
  (Fig. 47)


Polygonaceae                   External
  (Figs. 42-43)

Primulaceae                    Anatomical





Proteacceae                    Anatomical, external

Rhamnaceae                     Anatomical
  (Fig. 45)


Rhizophoraceae                 External


Rubiaceae                      Anatomical





Rutaceae                       Anatomical





Salvadoraceae                  External





Sapindaceae                    External


Sarcolaenaceae                 External






Scyphostegiaceae               External






Simaroubaceac                  Anatomical, external






Stackhousiaceae                External




Tamaricaceae                   Anatomical, External





Thymelaeaceac                  Anatomical, External



Turneracceae                   External



Vitaceac (including Leeaceae)  External
  (Fig. 44)


Zygophyllaceae                 Anatomical





Family                         Description

Achariaceae                    "Glieder eines zweiten
                                 staminalkreises";
                                 staminodes
Aextoxicaceae                  Fleshy, bilobed glands
                                 alternating with the
                                 stamens
Amaranthaceae                  Interstaminal appendages,
                                 staminodes



Apocybaceae (Figs. 48-49)      Nectaries derived from
                                 carpellodes


Bataceac                       Whitish spatulate,
                                 slender-stalked,
                                 denticulate "appendages"
                                 or staminodia; "Petalen
                                 die durchaus als
                                 staminodien gelten
                                 konnen"
Brassicaceae                   Transformed median
                                 stamens


Burseraceae                    A disk staminal in
                                 nature
Capparaceae                    Remnant of a former
                                 staminal supply,
                                 episepalous glands, or
                                 unilateral appendage
Celastraceae                   A disk of staminal
                                 nature (evidence of
                                 small traces)
Clusiaceae                     Transformed staminodes


Crassulaceae                   Staminodes or
                                 carpellodes

Ctenolophaceae                 Disk as modified
                                 stamens
Dichapetalaceae (Figs. 26-28)  Petals and disk lobes
                                 are staminodes

Dipentodonta-                  Staminodial(?)
  ceae                           nectary glands
Epacridaceae                   Staminodes repre-
                                 sented by a
                                 cluster of ante-
                                 petalous glands
                                 (1); or hair bun-
                                 dles on corolla
                                 tube (2)
Euphorbiaceae                  "Ecailles ou glan-
                                 des de nature
                                 staminodiale
                                 avec loges d'an-
                                 theres steriles"
                                 (1); staminodial
                                 origin of inner
                                 or outer whorl
                                 (3 stamen
                                 whorls) (2)
Fabaceae                       Disk as sterilized
                                 branches of the
                                 androecium

Flacourtiaceae                 Antepetalous
  (Figs. 36-                     staminode-like
  37, 39-40)                     disk append-
                                 ages: "stami-
                                 nodienartigen
                                 Diskus-
                                 forsatzen"
Francoaceae                    Staminodes



Geraniaceae                    Original triplo-
                                 stemony with
                                 transformation
                                 of outer stamen
                                 whorl
Greyiaceae (Figs. 10-11)       10 small staminodes

Humiriaccae                    "Des languettes etroites et
                                 subulees qui sont des filets
                                 depourvus d'antheres" (1); the
                                 disk can be interpreted as the
                                 inner sterilized part of the
                                 staminal tube (2); inner staminal
                                 whorls staminodial (3)
Hydrophyllaceae                "The nectary appears to be the
                                 morphologically homologous to an
                                 inner whorl of stamens"
Ixonanthaceae                  Disk of staminal origin
Lauraceae                      Splitting of organ in three parts
  (Fig. 41)                      and sterilization of lateral
                                 parts (1); result of association
                                 of three stamens
                                 and transforma-
                                 tion of lateral
                                 parts in glands
                                 (2); telomic
                                 structure (3)
Lepidobotrya-                  Staminodial disk
  ceae
Melianthaceae                  Posterior stamen
                                 as part of abax-
                                 ial nectary;
                                 "dass das hin-
                                 tere mediane
                                 Stamen fehlt,
                                 ... und zum
                                 Nectarhalter
                                 geworden ist"
Nyctaginaceae                  Interstaminal
                                 appendages
                                 interpreted as
                                 aborted stamens
Ochnaceae                      Staminodial disk,
                                 outer stami-
                                 nodes (corona)




Olacaceae (b)                  Staminodes


Opiliaceae                     Scales alternating
                                 with the sta-
                                 mens





Oxalidaceae                    Tongue-like structures
                                 separated from the back
                                 of the alternipetalous
                                 stamens
Paeoniaceae                    "The disk is largely
                                 androecial in nature"
                                 (1); "the disk
                                 represents a sterlised
                                 park of the androccium"
                                 (2)
Passifloraceae (c)             Staminodes as
                                 "Spitzchen... die sich
                                 als Staminod. deuten
                                 lassen (1); corona
                                 partly staminodial
                                 (limen) (2); 5
                                 alternating ridges in
                                 Basananthe; two whorls
                                 of 5 protrusions in
                                 Crossostema interpreted
                                 as original
                                 triplostemony (3)
Peridiscaceae                  Multilobed disk of
                                 staminodial origin
Podostemonaceae                The sepal-like staminodes
                                 arise at the base of the
                                 filament
Polemoniaceae                  5 Vestigial antepetalous
  (Fig. 47)                      stamen traces split up in
                                 numerous small branches and
                                 supply disk
Polygonaceae                   "Les nectaires isloles sont
  (Figs. 42-43)                  des etamines reduites"

Primulaceae                    A third whorl of vestigial
                                 traces (1); as petal marginal
                                 traces derived from the
                                 dorsal sepal trace and
                                 incorporated in the
                                 corolla (2)
Proteacceae                    Intrastaminal
                                 scales (e)
Rhamnaceae                     Disk from modified stamens
  (Fig. 45)                      (evidence of obdiplostemony)


Rhizophoraceae                 Inner whorl of staminodes
                                 alternating with the stamens
                                 in 3 of the 10 species (f)
Rubiaceae                      "The disk may
                                 represent an ex-
                                 pansion of the
                                 receptacle, or a
                                 second whorl of
                                 carpels"
Rutaceae                       Sterilized branches
                                 of the androe-
                                 cium, branches
                                 from staminal
                                 straces (modi-
                                 fied stamens)
Salvadoraceae                  Antepetalous
                                 "Zahnchen oder
                                 Diskus-Drusen"



Sapindaceae                    5 alternipetalous
                                 staminodes

Sarcolaenaceae                 Disk with "cinq
                                 ecailles al-
                                 ternisepales"
                                 (1); nectary disk
                                 of probable sta-
                                 minodial origin
                                 (2)
Scyphostegiaceae               Three stubs in
                                 front of the in-
                                 ner perianth and
                                 opposite the sta-
                                 mens (related to
                                 petals) (1); or
                                 stamens (2)
Simaroubaceac                  Variously receptacular
                                 derived from
                                 antesepalous stammens,
                                 or mixed antepetalous
                                 and carpellary traces;
                                 outer whorl of sterile
                                 carpels
Stackhousiaceae                "Die Drusen selbst
                                 entsprechen
                                 moglicherweise
                                 einem zweiten
                                 Staminalkreis"
Tamaricaceae                   "The disc is staminal in
                                 nature being formed by
                                 the staminal bases and
                                 their stripules" (1);
                                 inner antipetalous
                                 staminal whorl (2)
Thymelaeaceac                  Disk is the inner part of
                                 androecium


Turneracceae                   5 glands or protuberances
                                 between the stamens and
                                 petals

Vitaceac (including Leeaceae)  Staminodial tube,
  (Fig. 44)                      staminodial scales


Zygophyllaceae                 Disk of staminodial
                                 nature (vascular supply
                                 derived from stamen
                                 traces)

                               Protagonist
Family                         authority

Achariaceae                    Goldberg, 1986; Hooker &
                                 Masters 1871, cited in
                                 Harms, 1925b
Aextoxicaceae                  Ronse Decraene, 1985;
                                 Smets, 1988a

Amaranthaceae                  Joshi, 1932; Joshi &
                                 Venkata Rao, 1934;
                                 Saunders, 1939


Apocybaceae (Figs. 48-49)      Woodson and Moore, 1938



Bataceac                       Eckardt, 1959: 416,
                                 Johnson, 1935: 23





Brassicaceae                   Alexander, 1952;
                                 Bernhardi, 1838, cited
                                 in Eichler, 1878;
                                 Goebel, 1933
Burseraceae                    Shukla, 1995, cited in
                                 Narayana, 1960
Capparaceae                    Stoudt, 1941; Weberling
                                 & Uhlarz, 1983


Celastraceae                   Berkeley, 1953


Clusiaceae                     Eicher, 1878; Payer,
                                 1857; Ronse Decraene &
                                 Smets, 1991a
Crassulaceae                   Eichler, 1878


Ctenolophaceae                 Narayana & Rao, 1971

Dichapetalaceae (Figs. 26-28)  Breteler, 1973


Dipentodonta-                  Cronquist, 1981
  ceae
Epacridaceae                   Chatin, 1873b (1);
                                 Cronquist,
                                 1981; Eichler,
                                 1875 (2)



Euphorbiaceae                  Baillon, 1862b (1);
                                 Eichler, 1878;
                                 Gandhi &
                                 Thomas, 1983;
                                 Goebel, 1933;
                                 Michaelis,
                                 1924 (a) (2)



Fabaceae                       Moore, 1936a,
                                 1936b


Flacourtiaceae                 Eichler, 1878;
  (Figs. 36-                     Gilg, 1925;
  37, 39-40)                     Ronse De-
                                 craene, unpubl.



Francoaceae                    Bensel & Palser,
                                 1975b; Takhta-
                                 jan, 1997

Geraniaceae                    Dawson, 1936;
                                 Kumar, 1976



Greyiaceae (Figs. 10-11)       Cronquist, 1981; Dahlgren & Van
                                 Wyk, 1988; Steyn et al. 1987
Humiriaccae                    Baillon, 1860a: 208 (1); Narayana &
                                 Rao, 1969, 1977b: 150, 1978 (2);
                                 Winkler, 1931 (3)




Hydrophyllaceae                Cosa, 1995, cited in Sersic &
                                 Cocucci, 1999: 402

Ixonanthaceae                  Narayana & Rao, 1966
Lauraceae                      Daumann, 1931 (1); Eames, 1961,
  (Fig. 41)                      etc. (2); Rohwer, 1994 (3)







Lepidobotrya-                  Narayana & Rao,
  ceae                           1974
Melianthaceae                  Eichler, 1878;
                                 Wydler, 1863:
                                 149






Nyctaginaceae                  Buxbaum, 1961;
                                 Friedrich, 1956


Ochnaceae                      Cronquist, 1981;
                                 Gilg, 1925;
                                 Goebel, 1933;
                                 Saunders, 1939



Olacaceae (b)                  Sleumer, 1935


Opiliaceae                     None







Oxalidaceae                    Kumar, 1976



Paeoniaceae                    Eames, 1953, 1961
                                 (1); Goebel, 1933;
                                 Melville, 1984 (2)



Passifloraceae (c)             Harms, 1925a: 480 (1);
                                 puri, 1948, 1951 (2);
                                 De Wilde, 1974 (3)









Peridiscaceae                  Cronquist, 1981;
                                 Hutchinson, 1959
Podostemonaceae                Khosla & Mohan
                                 Ram, 1993:257

Polemoniaceae                  Dawson, 1936
  (Fig. 47)


Polygonaceae                   Emberger, 1936: 591
  (Figs. 42-43)

Primulaceae                    Dickson, 1936 (1);
                                 Saunders, 1939
                                 (2); Subramamyam &
                                 Narayana, 1976


Proteacceae                    Ronse Decraene, 1985

Rhamnaceae                     Nair & Sarma, 1961;
  (Fig. 45)                      Prichard, 1955


Rhizophoraceae                 Setoguchi et al., 1996


Rubiaceae                      Blaser, 1954: 538





Rutaceae                       Tillson & Bam-
                                 ford, 1938




Salvadoraceae                  Mattfeld, 1960a:
                                 232; Ronse De-
                                 craene, 1985



Sapindaceae                    Bonnier, 1879,
                                 cited in Smets,
                                 1988a
Sarcolaenaceae                 Baillon, 1884 (1);
                                 Cronquist, 1981
                                 (2)




Scyphostegiaceae               Baehni, 1937,
                                 1938 (1);
                                 Swamy, 1953,
                                 all cited in
                                 Heel, 1967 (2)


Simaroubaceac                  Ejehler, 1878;
                                 Engler, 1931c;
                                 Nair & Joseph,
                                 1957; Nair &
                                 Joshi, 1958


Stackhousiaceae                Mattfeld, 1960b:
                                 243



Tamaricaceae                   Murty, 1954: 235 (1)
                                 (1); Zohary &
                                 Baum, 1965 (2)



Thymelaeaceac                  Domke, 1934; Heinig,
                                 1951; Meisner,
                                 cited in Gilg,
                                 1984
Turneracceae                   Cronquist, 1981:
                                 409; Ronse
                                 Decraene, 1985

Vitaceac (including Leeaceae)  Nair & Nambisan,
  (Fig. 44)                      1957; Ridsdale,
                                 1974; Suessenguth,
                                 1953b
Zygophyllaceae                 Nair & Jain, 1956




                               Detractive
Family                         evidence

Achariaceae                    Ontogenetic, but
                                 vascularized

Aextoxicaceae                  External


Amaranthaceae                  No evidence for extra
                                 whorl of stamens



Apocybaceae (Figs. 48-49)      Anatomical, derivation of
                                 disk traces well below
                                 ovary

Bataceac                       Lacking; ontogeny needed






Brassicaceae                   Ontogeny, external,
                                 anatomical


Burseraceae                    None

Capparaceae                    External, ontogenetic



Celastraceae                   None


Clusiaceae                     Ontogeny


Crassulaceae                   External, ontogeny


Ctenolophaceae                 External, anatomical

Dichapetalaceae (Figs. 26-28)  External


Dipentodonta-                  None
  ceae
Epacridaceae                   Ontogenetic






Euphorbiaceae                  External, anatomi-
                                 cal








Fabaceae                       External, ontoge-
                                 netic


Flacourtiaceae                 Ontogenetic
  (Figs. 36-
  37, 39-40)




Francoaceae                    Ontogenetic, ana-
                                 tomical


Geraniaceae                    Ontogenetic, ana-
                                 tomical



Greyiaceae (Figs. 10-11)       Ontogenetic, anatomical

Humiriaccae                    Anatomical; ontogeny
                                 lacking





Hydrophyllaceae                None


Ixonanthaceae                  Ontogeny lacking
Lauraceae                      Ontogenetic
  (Fig. 41)







Lepidobotrya-                  External
  ceae
Melianthaceae                  Ontogenetic, ana-
                                 tomical







Nyctaginaceae                  Ontogenetic



Ochnaceae                      External






Olacaceae (b)                  External


Opiliaceae                     External







Oxalidaceae                    Anatomical, developmental



Paeoniaceae                    Developmental





Passifloraceae (c)             Developmental











Peridiscaceae                  No ontogenetic
                                 evidence
Podostemonaceae                External


Polemoniaceae                  None
  (Fig. 47)


Polygonaceae                   External, anatomical
  (Figs. 42-43)

Primulaceae                    Ontogenetic, anatomical
                                 (Coris)




Proteacceae                    Developmental

Rhamnaceae                     External, developmental
  (Fig. 45)


Rhizophoraceae                 Developmental


Rubiaceae                      No ontogenetic or
                                 anatomical evi-
                                 dence



Rutaceae                       External





Salvadoraceae                  External





Sapindaceae                    External


Sarcolaenaceae                 None






Scyphostegiaceae               Anatomical






Simaroubaceac                  Anatomical






Stackhousiaceae                No ontogenetic or
                                 anatomical
                                 evidence


Tamaricaceae                   External,
                                 developmental




Thymelaeaceac                  External



Turneracceae                   External



Vitaceac (including Leeaceae)  Developmental
  (Fig. 44)


Zygophyllaceae                 Developmental





Family                         Description

Achariaceae                    Nectary-like bodies


Aextoxicaceae                  5 pairs of coalescent
                                 glands derived from 10
                                 initial structures
Amaranthaceae                  "Nebenblatter" (1);
                                 pseudostaminodia
                                 (interstaminal
                                 appendages, part of
                                 staminal tube) (2)
Apocybaceae (Figs. 48-49)      "Proliferation of
                                 receptacular tissue
                                 between the androecium
                                 and the gynoecium"
Bataceac                       No conclusive evidence
                                 for staminodes or petals





Brassicaceae                   Receptacular nectaries
                                 with variable
                                 development and
                                 vascular connections
Burseraceae                    None

Capparaceae                    Late appearance in
                                 ontogeny, outer
                                 morphology

Celastraceae                   None


Clusiaceae                     Receptacular emergences


Crassulaceae                   Receptacular appendages,
                                 dorsal appendages of
                                 carpels
Ctenolophaceae                 Extrastaminal,
                                 receptacular
Dichapetalaceae (Figs. 26-28)  Nectary glands, disk
                                 lobes

Dipentodonta-                  None
  ceae
Epacridaceae                   "Le disque n'est
                                 que le gonfle-
                                 ment de la par-
                                 tie du receptacle
                                 qui supporte
                                 l'ovaire"

Euphorbiaceae                  Variably episepa-
                                 lous or epipeta-
                                 lous disk lobes
                                 with vascular
                                 supply from dif-
                                 ferent sources




Fabaceae                       Very late initiation
                                 of disk, diplo-
                                 stemonous
                                 flowers
Flacourtiaceae                 Scales are of same
  (Figs. 36-                     number as sta-
  37, 39-40)                     mens and ap-
                                 pear much later



Francoaceae                    No vascular con-
                                 nection, late ini-
                                 tiation,
                                 extrastaminal
Geraniaceae                    Basically diplo-
                                 stemonous, nec-
                                 taries
                                 receptacular

Greyiaceae (Figs. 10-11)       No vascular connection, late
                                 initiation, extrastaminal
Humiriaccae                    Disk variously supplied by bundless
                                 from the stamens, or without
                                 vascular connections




Hydrophyllaceae                None


Ixonanthaceae                  None
Lauraceae                      De novo emergences, staminal
  (Fig. 41)                      appendages







Lepidobotrya-                  Receptacular disk
  ceae
Melianthaceae                  No evidence for
                                 staminodial
                                 nature






Nyctaginaceae                  Extensions of the
                                 staminal tube


Ochnaceae                      Paracorolla as in
                                 Passifloraceae
                                 (no transition
                                 with stamens),
                                 next to true an-
                                 tepetalous sta-
                                 minodial whorl
Olacaceae (b)                  Extrastaminal or
                                 intrastaminal
                                 disk
Opiliaceae                     "Glandes volumin-
                                 euses" (1);
                                 intrastaminal
                                 nectary disk (2);
                                 "five broad disk
                                 lobes alternate
                                 with the sta-
                                 mens" (3)
Oxalidaceae                    Extrastaminal appendage or
                                 gland, ligular appendage


Paeoniaceae                    Receptacular disk





Passifloraceae (c)             Extrastaminal nectary
                                 receptacular in nature;
                                 also the 5 antesepalous
                                 nectarics of Adenia (no
                                 positional and time
                                 relation with the
                                 androccium); 5 alternating
                                 ridges dubiously staminodial




Peridiscaceae                  None

Podostemonaceae                Petaloid, spathulatetepals


Polemoniaceae                  None
  (Fig. 47)


Polygonaceae                   Receptacular mamillae
  (Figs. 42-43)

Primulaceae                    No external evidence





Proteacceae                    Nectar scales as
                                 secondary organs
Rhamnaceae                     Variable intrastaminal
  (Fig. 45)                      disk, intrastaminal
                                 thickening of the
                                 receptacle
Rhizophoraceae                 Instrastaminal
                                 appendages

Rubiaceae                      None





Rutaceae                       Enlargement of the
                                 floral axis be-
                                 tween the sta-
                                 mens and the
                                 base of the
                                 ovary
Salvadoraceae                  Considered as
                                 fused stipules of
                                 the stamens (1);
                                 receptacular na-
                                 ture (no vascu-
                                 lar supply) (2)
Sapindaceae                    Disk with 5 long,
                                 fleshy append-
                                 ages
Sarcolaenaceae                 Evidence is lack-
                                 ing to assign a
                                 staminodial na-
                                 ture to the disk



Scyphostegiaceae               Extrastaminal disk
                                 glands





Simaroubaceac                  Supply of disk
                                 highly variable in
                                 the family (g)




Stackhousiaceae                None




Tamaricaceae                   Stipular appendages
                                 ("Stipularzahnche-
                                 n"), staminal tube
                                 with teeth


Thymelaeaceac                  "Receptaculareffig
                                 ura-tionen" (no
                                 evidence of
                                 transitions)
Turneracceae                   Nectar secreted by
                                 broadened abaxial
                                 parts of filaments
                                 (nectarotheca)
Vitaceac (including Leeaceae)  Disk arising from
  (Fig. 44)                      the base of the
                                 gynoecium

Zygophyllaceae                 Receptacular
                                 emergence



                               Detractive
Family                         authority

Achariaceae                    Bernhard, 1999b


Aextoxicaceae                  Baillon, 1870


Amaranthaceae                  Eichler, 1878 (1);
                                 Eliasson, 1988; Payer,
                                 1857; Schinz, 1934 (2)


Apocybaceae (Figs. 48-49)      Rao & Arati Ganguli,
                                 1963: 433


Bataceac                       None






Brassicaceae                   Arber, 1931; Bowman &
                                 Smyth, 1998; Eichler,
                                 1878; Norris, 1941,
                                 etc.
Burseraceae                    None

Capparaceae                    Pax & Hoffmann, 1936;
                                 Payer, 1857; Weberling
                                 & Uhlarz, 1983

Celastraceae                   None


Clusiaceae                     Leins, 1964


Crassulaceae                   Eichler, 1878; Payer,
                                 1857; Smets, 1988a

Ctenolophaceae                 Link, 1992

Dichapetalaceae (Figs. 26-28)  Cronquist, 1981;
                                 Leenhouts, 1956, cited
                                 in Breteler, 1973
Dipentodonta-                  None
  ceae
Epacridaceae                   Payer, 1857: 578;
                                 Smets, 1988a





Euphorbiaceae                  Baillon, 1874;
                                 Beille, 1901;
                                 Venkatao Rao
                                 & Ramalak-
                                 shmi, 1968





Fabaceae                       Smets, 1988a



Flacourtiaceae                 Bernhard & En-
  (Figs. 36-                     dress, 1999
  37, 39-40)




Francoaceae                    Ronse Decraene &
                                 Smets, 1999


Geraniaceae                    Payer, 1857; Sat-
                                 tler, 1973;
                                 Smets, 1988a


Greyiaceae (Figs. 10-11)       Ronse Decraene & Smets, 1999

Humiriaccae                    Smets, 1988a, this study (based on
                                 descriptions in Narayana & Rao,
                                 1977b)




Hydrophyllaceae                None


Ixonanthaceae                  None
Lauraceae                      Endress, 1980; Kasapligil, 1951;
  (Fig. 41)                      Payer, 1857; Singh & Singh, 1985







Lepidobotrya-                  Link, 1991
  ceae
Melianthaceae                  Payer, 1857;
                                 Ronse Decraene
                                 et al., 2001






Nyctaginaceae                  Rohweder &
                                 Huber, 1974;
                                 Vanvincken-
                                 roye et al., 1993
Ochnaceae                      Eichler, 1878;
                                 this study





Olacaceae (b)                  Cronquist, 1981;
                                 Reed, 1955;
                                 Smets, 1988a
Opiliaceae                     Baillon, 1892: 412
                                 (1); Cronquist,
                                 1981 (2); Reed,
                                 1955: 41 (3)




Oxalidaceae                    A1-Nowaihi & Khalifa, 1971;
                                 Eichler, 1878


Paeoniaceae                    Baillon,, 1862; Eichler,
                                 1878; Hiepko, 1966




Passifloraceae (c)             Bernhard, 1999a











Peridiscaceae                  None

Podostemonaceae                Baillon, 1886; Engler, 1930a;
                                 Rutishauser, 1997 (d)

Polemoniaceae                  None
  (Fig. 47)


Polygonaceae                   Ronse Decraene & Akeroyd,
  (Figs. 42-43)                  1988; Ronse Decraene
                                 & Smets, 1991c
Primulaceae                    Payer, 1857;
                                 Ronse Decraene
                                 et al., 1995



Proteacceae                    Brough, 1933; Douglas
                                 & Tucker, 1996
Rhamnaceae                     Bennek, 1958; Payer,
  (Fig. 45)                      1857; Suessenguth, 1953a


Rhizophoraceae                 Juncosa, 1988; Juncosa &
                                 Tomlinson, 1987

Rubiaceae                      None





Rutaceae                       Penzig, 1887,
                                 cited in Tillson
                                 & Bamford,
                                 1938


Salvadoraceae                  Gluck, 1919, cited
                                 in Mattfeld,
                                 1960a (1);
                                 Kshetrapal,
                                 1970 (2)

Sapindaceae                    Radlkofer, 1896


Sarcolaenaceae                 Smets, 1988a






Scyphostegiaceae               Van Heel, 1967






Simaroubaceac                  Smets, 1988a






Stackhousiaceae                None




Tamaricaceae                   Eiehler, 1878;
                                 Payer, 1857




Thymelaeaceac                  Gilg, 1894



Turneracceae                   Smets, 1988a



Vitaceac (including Leeaceae)  Gerrath Ct al., 1990
  (Fig. 44)


Zygophyllaceae                 Ronse Decraene,
                                 unpubl. obs.



(a)Michaelis (1924) gives several arguments for a staminodial nature of
the nectaries, including the position of the glands and external shape.
The late initiation and variable position of the nectaries (e.g.,
Beille, 1901) are arguments against this.

(b)True staminodes occur occasionally in the Olacaceae (e.g., Agarwal,
1963; Baitlon, 1892; Sleumer, 1935: Olax, Liriosma). In some genera of
tribes Anacoloseae and Aptandreae there are disklike appendages with a
possible homology to stamens (Sleumer, 1935:7: "Es konnte sich bei diesn
lappigen Drusen oder dem gekerbten Drusenring auch um umgebildete
aussere oder inner Stam. handeln").

(c)In Crossostemma and Basananthe a second series of small protrusions
alternates with the stamens (Bernhard, 1999a).

(d)Podostemoideae posses an additional envelope, homologous to prophylls
or leaves (spathella), whereas Tristichoideac have a cuplike cover
(Cupule) (Rutishauser, 1997.)

(e)Haber (1959, 1961, 1966) interprets the scales as a petal whorl,
because their vasculature is connected with the sepal lateral bundles,
their tetramerous plan, and the alternisepalous position. Joshi (1936)
interprets the disk scales of Stellera (Thymclacaceae) in the same way.

(f)The "staminodes" in Crossostylis alternate with the stamens and are
the same in number. They have no vascular connection and no obvious
function. They are situated between the stamens and a nectary disk that
is present in all species (Setoguchi et al., 1996). Juncosa (1988: 86)
states that the intrastaminal appendages are initiated long after the
stamens have developed and are therefore "clearl not staminodes." The
common diplostemonous androecium in the family (symplesiomorphy)
supports the latter interpretation.

(g)The disk of Brucea receives its vascular supply from the three
sources: branches from the antesepalous staminal traces, a first whorl
of disk traces is found alternating with the stamens, followed by a
second whorl opposite the stamens, but as a part of the carpellary
tissue (Nair & Joshi, 1958). Engler (1931c) described Alvaradoa as
having five sterile antepetalous stamens. In other cases (e.g.,
Eurycoma) the description of antepetalous ("wahrscheinlich Staminodien":
1.c.: 381).
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Author:Decraene, L.P. Ronse; Smets, E.F.
Publication:The Botanical Review
Geographic Code:1USA
Date:Jul 1, 2001
Words:20846
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