Calceolariaceae: floral development and systematic implications

CALCEOLARIACEAE: FLORAL DEVELOPMENT AND

SYSTEMATIC IMPLICATIONS1

EVA M. MAYR AND ANTON WEBER2

Center of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria

The recent establishment of the new family Calceolariaceae, separated from Scrophulariaceae on the basis of molecular

evidence, is complemented here by a scanning electron microscopy study of floral morphology and development of 12 species

encompassing all genera (Calceolaria, Jovellana, and Stemotria [¼ Porodittia]). All species showed a similar pattern of organ

initiation. The slightly zygomorphic, four-merous calyx is the first floral organ series initiated, with the primordia emerging

consecutively in a unidirectional (dorso-ventral) succession. The two entire corolla lips in Calceolaria and Jovellana arise as

uniform meristematic ridges (sometimes with a central emargination, especially in Jovellana), kept apart by two lateral stamen

primordia. Later the margins of the lips fuse across the backs of the young stamens, giving rise to the short corolla tube (late

sympetaly). Stemotria stands out by having three stamens instead of two and a bilobed lower lip, resulting in a trimerous corolla.

Similar architecture was found in teratological flowers of Calceolaria. The perianth of Calceolariaceae is shown to be derived

from a tetramerous condition, not from pentamery as traditionally believed. This is in agreement with the separation of

Calceolariaceae from Scrophulariaceae and with their placement in succession of Oleaceae and Tetrachondraceae in the basal

Lamiales. The hitherto puzzling molecular evidence is thus supported by morphological–developmental features of the flower.

Key words: Calceolaria; Calceolariaceae; floral development; Jovellana; Lamiales; Stemotria (¼ Porodittia).

The three genera Calceolaria, Jovellana, and Stemotria (¼Porodittia) traditionally have been placed in the familyScrophulariaceae in which they formed a distinct group (rankedas tribe: e.g., Don, 1835; Bentham, 1846, 1876; Wettstein,1891; Kranzlin, 1907; Melchior, 1964; as subtribe: Lemaire,1856; or as subfamily: Luersson, 1882), but their relationship toother groups has remained unclear. Their position in theScrophulariaceae depends largely on the definition of thatfamily. Until the advent of molecular systematics, Scrophular-iaceae represented a large, morphologically heterogenousgroup, which had long been thought to be artificial (e.g.,Thieret, 1967; Burtt, 1965; Hartl, 1955, 1965–1974). Recentmolecular studies (Olmstead and Reeves, 1995; Young et al.,1999; Olmstead et al., 2001; Oxelman et al., 2005) definitivelyproved their polyphyly, and Scrophulariaceae were split intoseveral families. One of these newly established groups was thefamily Calceolariaceae, comprising the three genera Calceo-laria, Jovellana, and Stemotria (¼Porodittia) (Olmstead et al.,2001). Calceolariaceae proved not only unrelated to the othersegregates of Scrophulariaceae (e.g., Scrophulariaceae sensustricto, Plantaginaceae¼ ‘‘Veronicaceae’’, Stilbaceae), but alsoplaced in a basal position within the Lamiales, preceding theGesneriaceae and the odd genera Sanango and Peltanthera, andfollowing the Oleaceae and Tetrachondraceae (Albach et al.,2001; Bremer et al., 2001, 2002).

In the present study we investigated how floral morphologyand development fit into this picture. While many studies (e.g.,Bentham, 1846; Eichler, 1875; Wettstein, 1891; Kranzlin,1907; Rendle, 1925; Lawrence, 1951; Melchior, 1964; Vogel,1974; Sersic, 2004) related the floral morphology ofCalceolaria and its allies to that of typical Scrophulariaceae,other authors have pointed out problems in doing so(Schumann, 1890; Varghese, 1967; Endress, 1999). Areinvestigation on a broader scale, that is, one including allgenera of Calceolariaceae with an emphasis on floral de-velopment, thus seemed necessary.

MATERIALS AND METHODS

The study includes 12 species of Calceolariaceae, covering all genera(Calceolaria, Jovellana, and Stemotria¼ Porodittia). Inflorescences and floralbuds were obtained from field collections (Costa Rica), cultivated plants, andherbarium material. Voucher specimens of field-collected species weredeposited at the Herbarium of the University of Vienna, Vienna, Austria (WU).

SEM techniques—Inflorescences were fixed and preserved in 70% ethanoland dehydrated in FDA (formaldehyde dimethyl acetal) (Gerstberger and Leins,1978). Herbarium material (Stemotria triandra) was soaked in a 6 : 1 mixtureof 10% aqueous aerosol OT (dioctyl sodium sulfosuccinate) and 95% acetone(Peterson et al., 1978). The specimens prepared for SEM were dissected undera stereomicroscope, critical point dried (Balzers 030 critical point dryer, BalzersAG, Liechtenstein), mounted on stubs with customary nail varnish, and sputter-coated with gold in an argon atmosphere (Balzers sputter coater). The sampleswere viewed and photographed at 10 and 15 kV in a JEOL (Peabody,Massachusetts, USA) 35-CF scanning electron microscope.

Plant material—The following specimens were used: Calceolariachelidonioides Kunth, cult. HB Vienna (HBV) (from HB Duisburg (DUIS),no. 742); C. glandulosa Benth., cult. HB Munich (MSB), leg. C. Ehrhart; C.irazuensis Donn. Sm., Costa Rica, Cerro de la Muerte, leg. E. M. Sehr & E. M.Mayr 20040220/01 (WU); C. mexicana Benth., Costa Rica, Cerro de la Muerte,leg. E. M. Sehr & E. M. Mayr 20040220/02 (WU); C. mexicana Benth., cult.HB Vienna (HBV) (from HB Graz (GZU), no. 783); C. nevadensis Standl.,cult. HB Munich (MSB), Wei 3659, leg. C. Ehrhart. C. tripartita Ruiz & Pav.,cult. HB Vienna (HBV) (from Stuttgart (HOH), no. 1416); C. viscosissimaLindl., cult. HB Munich (MSB), leg. C. Ehrhart; Jovellana punctata Ruiz &Pav., cult. HB Munich (MSB), leg. C. Ehrhart; J. punctata Ruiz & Pav., cult.

1 Manuscript received 13 June 2005; revision accepted 6 December 2005.

The authors thank Dr. C. Ehrhart (University of Munich, Germany), Dr.M. Moeller (Royal Botanic Garden Edinburgh, UK), Prof. Dr. U. Molau(Gothenburg, Sweden) and Dipl. Biol. A. Schmidt-Lebuhn (University ofGottingen, Germany) for providing fixed material and/or photographs forstudy; Mag. S. Sontag and A. Glaser for SEM assistance and technicalsupport; Drs. W. Huber, A. Weissenhofer, R. Buchner, and M. Weber forsupport and information; and the Botanical Garden of the University ofVienna (HBV) and the Horticultural Division of the Royal Botanic GardenEdinburgh (RBGE) for caring for plant material. Special thanks go to twoanonymous reviewers who contributed to substantial improvement of thepaper.

2 Author for correspondence (e-mail: [email protected])

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American Journal of Botany 93(3): 327–343. 2006.

HB Edinburgh (RBGE), no. 19980699, leg. M. Moeller; J. sinclairii Kraenzl.,cult. HB Edinburgh (RGBE), no. 19330356, leg. M. Moeller; J. violacea G.Don, cult. HB Munich (MSB), leg. C. Ehrhart; J. violacea G. Don, HBEdinburgh (RBGE), no. 19684917, leg. M. Moeller; Stemotria triandra Wettst.& Harms, Herbarium HB Chicago (F), Peru, Ancash, Prov. Yungay, leg.Dillon, Molau & Matekaitis.

RESULTS

Floral organography of Calceolaria—The flowers aredistinctly zygomorphic, have a four-parted calyx, with thelobes free to the base, and a two-lipped sympetalous corolla.The two stamens, in a transverse position, are fused to a shortcorolla tube, which encloses the bicarpellate-syncarpousgynoecium. Illustrations of the flowers of many species canbe found in Vogel (1974), Ehrhart (2000), and Sersic (2004).

The four-parted calyx is consistent within the genus. Theadaxial calyx lobe is larger than the lateral pair, and the abaxiallobe remains the smallest. Thus, the calyx appears slightlyzygomorphic. It is usually green and persistent. The aestivationof the lobes is valvate.

The two-lipped corolla is mostly yellow, rarely white, red, orviolet, and often bears markings of variable shape and color(red to purple). The upper and the lower lips are connate attheir base and form a short corolla tube. The shape of thecorolla is highly variable and can be grouped into several types(Ehrhart, 2000). The upper lip is usually arched or hooded andmuch smaller than the pouched lower lip. The majority ofspecies has oil flowers. Their inflated lower lip has an infoldedmedian lobe, bearing a patch of densely arranged oil-secretingtrichomes. This ‘‘trichome-elaiophore’’ secretes fatty oil in themature flower, which is gathered by oil-collecting bees(Tapinotaspis and Centris spp.; Vogel, 1974). In some species,oil glands are missing and the flowers either offer pollen (butnever nectar) to their visitors or are autogamous (Vogel, 1974).

The stamen pair is placed in episepalous-transversalposition. The filaments are inserted at the base of the corollatube. The anthers are ultimately two-celled, but the cells maybe almost completely confluent in some species of sect.Micranthera (Molau, 1988).

The gynoecium consists of two median, fused carpels, and issuperior to semi-inferior (Hartl, 1955). The style terminates inan inconspicuous or slightly capitate stigma. The fruit is a drycapsule of ovoid-conical shape; dehiscence is septicidal andloculicidal. The capsule bears numerous tiny, striate seeds.

In this study, the floral development of only two species, C.glandulosa and C. viscosissima, is documented in detail.According to Ehrhart (2000), both belong to sect. Cheiloncos;C. viscosissima is a member of the C. integrifolia complex(Ehrhart, 2005). In the other species (C. chelidonioides, C.irazuensis, C. mexicana, C. nevadensis), development does notdiffer remarkably. In the following descriptions, the adaxialand abaxial side of the flower will be referred to as upper andlower side, respectively.

Floral development of Calceolaria glandulosa—The four-merous calyx is the first floral organ series initiated. The sepalprimordia originate unidirectionally in an adaxial to abaxialdirection. The upper sepal primordium is first and largest,followed by the two lateral sepals, which emerge more or lesssimultaneously, and finally the lower sepal primordium arises(Fig. 1a–c).

Throughout development, the upper sepal appears larger

than the lateral pair, while the lower sepal consistently remainsthe smallest. The two lateral sepals enlarge evenly untilanthesis. When sepal initiation is completed, trichomes beginto grow out from the outer surface of the upper sepal (Fig. 1d).This stage of sepal development also marks the initiation of theinner organs. The enlarging sepals then curve over the center ofthe bud to protect the inner primordia, but do not forma completely closed bud. As development progresses,zygomorphy of the calyx becomes less pronounced (Fig. 1e–i) and is hardly discernible in the flower at anthesis.

The size differences of the sepals are also reflected in thewidth of insertion. Therefore, the plateau in the center of thefloral bud is much narrower on the abaxial side and hasa trapezoid form in outline (Fig. 1d, e).

The primordia of the corolla and the androecium arisesimultaneously (Figs. 1c–f, 2a). At first, a low circular moundemerges, surrounding a shallow median depression (Fig. 1c).

The two stamen primordia emerge as two ovoid bulges in theradii of the lateral calyx lobes (Fig. 2a). At early stages, theygrow comparatively fast, outgrowing the rim-shaped initials ofthe corolla (Fig. 2b, c). The enlarging stamens rapidly increasein circumference until their margins meet. Thus, theyconsistently keep the initials of the two corolla lips apart. Asgrowth proceeds, shallow vertical furrows become visible ontop of the stamen primordia (Fig. 2d). This marks thebeginning of anther differentiation and is quickly followedby the differentiation of a short filament.

The upper and lower corolla lips arise as transversal ridgeson either side of the floral apex. They are located above andbelow the stamens and in superposition to the upper and lowercalyx lobe, respectively. The two lip primordia emergeindividually, without any meristematic junction between them,and are separated by the young stamens (Fig. 2a–c). At earlystages of corolla development, when the stamens are stillhigher than the corolla, the upper lip appears slightly moreprominent than the lower lip (Fig. 2d).

Striking changes in corolla organogenesis occur at laterstages of anther differentiation. On the outer surface of theprospective filaments, a meristematic band arises, whichconnects the margins of the hitherto isolated corolla lips (Fig.3b), thus forming a short corolla tube (Fig. 3c). The youngstamens are enclosed by this newly formed meristematic ring,with their short filaments inserted at the base of the corolla tube(Fig. 3e).

When the corolla tube starts to form, the slightly larger upperlip is overtaken by the lower one. This tube elongates andcurves over the anthers like a hood (Figs. 2e, f; 3c, d). Thelower lip continues to be larger than the upper until anthesis.

By the time the lower lip has covered roughly the lower halfof the anthers, the upper lip has also enlarged and is nearly thesize of the lower lip (Fig. 3e). This process is preceded by theemergence of glandular trichomes on the outer surface of bothcorolla lips (Fig. 2g).

Shortly after glandular trichomes have started to emerge onthe outside of the corolla, the elaiophore becomes visible on thelower corolla lip (Figs. 2h, 3f). In the mature flower, it isrepresented by a broad band of densely arranged glandulartrichomes, which secrete a fatty oil. It is restricted to the centralpart of the upper border of the lower corolla lip.

Because the elaiophore is formed on the underside of thelower lip, an invagination is required to bring it in its functionalposition inside the calceolus. Zonal growth of the lower corollalip results in the required rearrangement. Beneath the

328 AMERICAN JOURNAL OF BOTANY [Vol. 93

prospective trichome-elaiophore, the hairless part of the corollasurface begins to bulge outward. Whereas the upper lip remainsrelatively short, the lower lip continues to expand and formsa saccate bulge (Fig. 2h, 3f). The enlarging bulge then foldsover the band-shaped elaiophore in an upward movement (Fig.3g). In this (late) stage, the onset of a slight tripartition of themargin of the lower lip can be seen, with the central lobebearing the elaiophore.

As a result of this enlargement, the median lobe bearing theelaiophore turns and folds into the extended lower lip.Compared to the large, inflated lower corolla lip, the upperlip remains relatively small and is arch-shaped.

The carpel primordia arise as two crescent-shaped ridges.The ridges grow upward and form the incipient ovary walls.The lateral flanks of the carpels broaden until their marginsmeet and form the septum (Fig. 4a, b). The apex of the younggynoecium tapers during early style formation (Fig. 4c, d). Asthe prospective style elongates, the terminal slit closes beforestigmatic papillae are initiated (Fig. 4d). Finally, the elongatingstyle terminates in a slightly clavate stigma, which comprisesnumerous papillae (Fig. 4e, f).

Floral development of Calceolaria viscosissima—Thefloral organs of C. viscosissima are similar to those of C.glandulosa in position and initiation. The development differsfrom C. glandulosa in rather insignificant features, such asproportions and growth rates. For that reason, the followingdescription mainly focuses on comparisons with that species.Most remarkable are the floral anomalies observed in C.viscosissima, especially the bipartition of the lower lip and thedevelopment of a third stamen.

The first noticeable difference between C. glandulosa and C.viscosissima is evident at a later stage of calyx development.After calyx initiation is completed and trichomes have startedto emerge from the outer surface, the young calyx lobes enlargeuntil their margins meet, then they closely curve over the floralapex. Unlike those of C. glandulosa, they cover the developinginner organ primordia completely (Fig. 5a–c).

The initiation of corolla and androecium in C. viscosissimalargely corresponds to that of C. glandulosa. There is,however, a slight difference in timing: the somewhat retardedcorolla catches up with the androecium even before the start ofanther differentiation (Fig. 5f). Also, the growth rate of thecorolla lips differs slightly. Whereas in C. glandulosa the upper

Fig. 1. SEM of Calceolaria glandulosa, calyx initiation and development. (a) Inflorescence apex with flower primordium and two subsequent flowerprimordia (fp). (b–c) Initiation of sepals (s) in adaxial to abaxial succession. (d–f) Further development of sepals (s), emergence of trichomes on their outersurface; initiation of corolla and stamens (st). (g–i) Sepals bending over developing corolla and androecium. All figures oriented with adaxial sepalprimordium above. Bar¼ 100 lm. Figure abbreviations: ct, corolla tube; e, elaiophore; fp, flower primordium; ll, lower lip; mst, median stamen; s, sepal;se, septum of gynoecium; st, stamen; ul, upper lip.

March 2006] MAYR AND WEBER—FLORAL DEVELOPMENT OF CALCEOLARIACEAE 329

lip is retarded and the lower lip develops precociously (Fig.2d–f), in C. viscosissima the two corolla lips bulge almostevenly over the anthers until the elaiophore starts to emerge(Figs. 5g–j, 6).

In C. viscosissima, many remarkable teratological flowershave been found. One common anomaly observed anddocumented at various developmental stages is that the lowercorolla lip appeared two-parted. The location and depth of thisdivision proved highly variable: the lower lip was eitherdivided into two equal fractions or was asymmetricallycleaved. In some cases, only a slight constriction occurred(Fig. 7a), whereas in others a deep fissure split the lip into twoparts (Fig. 7b, c). Frequently, the floral buds with an evenlydivided lower lip also developed a third stamen in lower-median position (Fig. 7d, e). In this case, the lip was alwaysdeeply incised. After anther differentiation, the orientation of

the median stamen could be easily determined; the two regularstamens retained their usual position, the additional stamen wasin a median position (Fig. 7f). This is most remarkable, as thefloral structure and position of the third stamen is similar inStemotria triandra (discussed later).

Organography of Jovellana—Principally, the flowers ofJovellana correspond to those of Calceolaria, but there areremarkable differences in the shape and color of the corolla (forillustrations of the three species investigated, see Table 4929 inW. Hooker [1856], Fig. 25F in Wettstein [1891], and Fig. 2Din Sersic [2004] for J. violacea; Table 5392 in W. Hooker[1863] for J. punctata; Table 6597 in J. D. Hooker [1882] forC. sinclairii).

The four-parted calyx is similar to that of Calceolaria. Thesepals are free to the base, and their aestivation is valvate. Due

Fig. 2. SEM of Calceolaria glandulosa, development of corolla and androecium; sepals (s) removed. (a–d) Growth of stamen primordia (st) and upper(ul) and lower corolla lip (ll). (e–f) Differentiation of anthers and basal fusion of corolla lips, formation of a short corolla tube (ct). (f–h) Enlargement ofcorolla lips, emergence of glandular trichomes and (h) oil glands (elaiophore, e). Bars a–g ¼ 100 lm, h¼ 500 lm.


to their differences in size, the calyx appears slightlyzygomorphic.

The two-lipped sympetalous corolla is violet to white orflushed yellow with purple to yellow markings. Both corollalips are entire, but unlike Calceolaria, protrude forwards andform an oblique bell, with a more or less involute margin. Theupper lip is not much smaller than the lower one, but issometimes shallowly emarginate. The lower corolla lip is neversaccate or pouched, and a median lobe (present in Calceolariaand bearing the elaiophore) is absent. Oil-producing trichomesare entirely missing. The flowers are visited by pollen-collecting bees and by oil-collecting bees that gather pollenonly (Vogel, 1974). The lips are connate at their base so thata short corolla tube is formed.

The stamen pair is placed in an episepalous-transversalposition. The short filaments are inserted near the base of theshort corolla tube. The anther cells are confluent.

The gynoecium is semi-inferior and consists of two median,fused carpels. The style is short and terminates in a capitatestigma. The fruit is a dry capsule of ovoid-conical shape withsepticidal and loculicidal dehiscence. The seeds are numerousand striate.

Floral development of Jovellana—The three investigatedspecies (J. punctata, J. sinclairii, J. violacea) are almostidentical in their floral development. Apart from minordifferences and the fact that oil glands are entirely missing,

the floral structure and development are also very similar tothose of Calceolaria.

Although we studied the complete floral development in J.punctata, this species tends to produce floral teratologies incultivation, making interpretation difficult. Therefore, we willfirst document the essential developmental stages for the calyxin J. sinclairii and for the corolla and androecium in J.violacea, then describe J. punctata.

Jovellana sinclairii—As in Calceolaria, the four calyx lobesemerge consecutively in adaxial to abaxial succession (Fig. 8a–c). Before initiation of the inner floral organs, trichomesemerge from the outer surface of the young sepals. Thisprocess starts on the upper calyx lobe and proceeds to thelateral lobes (Fig. 8c–e). The lower calyx lobe is the last one todevelop multicellular, eglandular trichomes. The upper andlateral calyx lobes enlarge increasingly, widening to the pointwhere their margins meet. Initially, the lower sepal developsmore slowly, but soon catches up (Fig. 8e, f). As developmentprogresses, the calyx lobes bend over the floral apex. Marginaltrichomes of the adjacent lobes interlock and seal the calyx ina protective way. Thus, the calyx covers the developing innerorgans almost completely (Fig. 8g, h). The calyx re-opens later,after the corolla and androecium are well developed and haveacquired their mature shape. Then the previous size differencesof the sepals become nearly indiscernible (Fig. 8i).

Fig. 3. SEM of Calceolaria glandulosa, stamen and corolla differentiation, floral buds in side view; sepals removed. (a–e) Formation of corolla tube(ct), differentiation of stamens (st), unequal development of upper (ul) and lower corolla lip (ll) lip. (d–e) Emergence of glandular trichomes. (f–g)Initiation of elaiophore (oil glands, e) and differentiation of lower lip. SEM micrographs. Bars a–d ¼ 100 lm, e–g¼ 500 lm.


Jovellana violacea—Corolla and androecium arise simulta-neously from an almost ring-shaped meristem in the center ofthe floral apex (Fig. 9a). The two stamen primordia emerge asshallow ovoid mounds in episepalous position (Fig. 9b). Thecorolla lips are initiated as meristematic ridges, that are moredistinct than in Calceolaria, and a depression occurs in thecenter of the upper and the lower lips. The emarginationdisappears in later stages (Fig. 9e, f) and is indiscernible in theanthetic flower.

As the lips enlarge, the undifferentiated stamen pair ispushed toward the center of the floral bud. Without appreciableenlargement, the stamen primordia meet in the middle. Duringthis process, a short corolla tube originates, with the stamenpair inserted at the junction of the lips (Figs. 9d–f, 10a, b).

After formation of the corolla tube, the upper and lower lipsstart to bulge over the stamen primordia (Fig. 9g). UnlikeCalceolaria, the upper lip grows faster than the lower one. Thesinus between the two lips narrows continuously and finally thecorolla closes (Fig. 10d, e). The margin of the upper lip slightlyoverlaps the lower, and glandular trichomes begin to grow outfrom their outer surface (Figs. 9h, i, 10f, g). Antherdifferentiation does not start until the corolla lobes overarchthe inner organs completely.

Jovellana punctata—Calyx initiation of J. punctata largelycorresponds to that of J. sinclairii. The most remarkabledifference concerns the trichomes on the outer surface of the

young sepals. Whereas filiform, eglandular trichomes areformed in J. sinclairii, J. punctata bears almost sessileglandular trichomes. Because interlocking trichomes aremissing, the calyx never closes completely over the developinginner floral organs.

The depression in the center of both corolla lips, observed inJ. violacea, proved even more pronounced in J. punctata.Especially in the lower lip, a rather deep fissure formed fairlyregularly. In many cases, this feature can also be observed inthe anthetic flower, causing a somewhat teratological appear-ance. Whether this is due to genetic instability of the cultivatedmaterial or is in the range of natural variation, is unknown tous. The late development of corolla and androecium is similarto J. violacea.

Organography of Stemotria triandra—The flowers of S.triandra (the only species in the genus Stemotria¼ Poroditta)differ from those of Calceolaria and Jovellana in the shape ofthe corolla and the presence of a third stamen. Before going intodetail, previous erroneous reports on the orientation of theflower must be discussed. Cavanilles (1799) was the first topresent an illustration of the species (as Jovellana triandra;reproduced in Fig. 11a–a"). His drawing of the flowers is,however, wrong in several respects: the corolla is shown ashaving two entire, somewhat pouched lips (and thus recallingthat of Jovellana), the third stamen is shown in an upper-medianposition, and all stamens are shown in a transverse orientation.

Fig. 4. SEM of Calceolaria glandulosa, initiation and development of gynoecium; calyx, corolla, and stamens (st) removed. (a–b) Emergence ofcarpels and formation of septum (se). (c) Upgrowth and closing of ovary. (d) Development of indumentum and differentiation of style. (e–f) Close-ups ofstigmatic area with developing stigmatic papillae (sp). Bars ¼ 50 lm.


Wettstein (1891) gave a similar verbal description, apparently

based on Cavanille’s description and drawings. Kranzlin (1907)

was the first to describe the tripartitioning of the corolla.

However, he thought that (as in typical Scrophulariaceae) the

two smaller lobes would represent the upper lip and the larger

one the lower lip (see Fig. 11b0). Also, Molau (1988) and E.

Fischer (2004) gave a similar description, but in Molau’s

illustration the flowers are shown in a reverse orientation (Fig.

11c, c0). In fact, these drawings, which contradict the text, are

the only ones that reflect the true orientation of the Stemotriaflowers. Our statements are based on photographs kindly

provided by Prof. Ulf Molau (Gothenburg, Sweden), herbarium

material, and flower development (see the following section).

As in Calceolaria and Jovellana (see Weber, 1973; Andersson

Fig. 5. SEM of Calceolaria viscosissima, floral development. Sepals removed in (d–l). (a–c) Calyx initiation and development; note sepals (s) bendingclosely over floral apex. (d–f) Initiation and early development of corolla and androecium; ul¼upper lip, ll¼ lower lip of corolla, st¼ stamen primordium.(g–i) Further development of corolla lips and differentiation of anthers; formation of short corolla tube (ct). (j–l) Enlargement of corolla lips, emergence ofglandular trichomes and (k) oil glands; further growth of lower lip and invagination of distal part bearing the elaiophore (e). Bars a–i¼ 100 lm, j–k¼ 400lm.


and Molau, 1980), the thyrsic inflorescences are composed ofpair-flowered cymes, with each flower pair comprisinga terminal and a front flower. Both flowers show equalorientation, with the large corolla lobe pointing upward. Thus,the large median lobe represents the upper lip and the smaller

lateral lobes the lower lip. The third stamen occupies a median-lower (abaxial) position (Fig. 12).

The four-parted calyx is similar to that of Calceolaria andJovellana. The zygomorphy is clearly discernible at earlystages of development, but is not very pronounced in the

Fig. 6. SEM of Calceolaria viscosissima, stamen and corolla differentiation; floral buds in side view, sepals (s) removed. (a–b) Formation of corollatube (ct), differentiation of stamens (st); ul¼ upper lip, ll¼ lower lip of corolla. (c–d) Development of corolla lips; emergence of glandular trichomes andoil glands of the elaiophore (e, arrow). (e–g) Enlargement of lower corolla lip and invagination of distal part bearing the elaiophore (e). Bars a–d¼100 lm,e–g ¼ 500 lm.

Fig. 7. SEM of Calceolaria viscosissima, teratological flowers; sepals removed. (a–c) Floral buds with (a) symmetrically or (b–c) asymmetricallydivided lower lips (ll); ul ¼ upper lip of corolla. (d–f) Buds with additional median stamen (mst) and two-parted lower lip. Bars ¼ 100 lm.


anthetic flower. The sepal lobes are free to the base and theiraestivation is valvate. The calyx is green and persistent.

The bright yellow corolla is zygomorphic and sympetalous.The entire upper lip and the bilobate lower lip are never saccate,arched or hooded, but spread patently. The three corolla lobesare almost equal in size, the upper slightly larger than the lowertwo. The upper and lower corolla lips are connate at their baseand form a short corolla tube. Oil-producing trichomes areentirely missing. There are no data on pollination.

The lateral stamen pair is placed in the episepalous-transversal position. The median stamen is abaxial insuperposition to the lower calyx lobe. The short filaments areinserted in a distinct, dark purple ring at the base of the corollatube. Before anthesis, the anthers have a dark, shining, almostmetallic appearance. They are two-celled and not confluent.

The gynoecium consists of two median, fused carpels and issurrounded by a short cupular corolla-tube. The conical ovaryhas numerous densely arranged glands on its outer surface. Thestyle terminates in a pointed stigma. The fruit is a dry capsuleof ovoid-conical shape; dehiscence is septicidal and loculicidal.The capsule bears numerous tiny, striate seeds.

Floral development of Stemotria triandra—As in Calceo-laria and Jovellana, the four-merous calyx of S. triandra is

initiated in adaxial to abaxial succession. Similarly, the adaxialprimordium is larger than the lateral pair, while the abaxialprimordium remains the smallest. Judging from the prominentglandular trichomes on their outside, the upper and lateral calyxlobes are already well developed when the lower one appears(Fig. 13a). Nonetheless, the size difference of the calyx lobessoon becomes less pronounced (Fig. 13b, c) and is almostindiscernible in the anthetic flower. When the calyx bends overthe top of the floral bud, the inner primordia start to emerge.

As in Calceolaria and Jovellana, the corolla and androeciumarise concurrently. A low circular mound, surroundinga shallow median depression, emerges from the trapezoidplateau in the center of the floral bud (Fig. 13d). Theprimordium of the upper corolla lip is entire, whereas twoseparate corolla lobes arise on the lower side of the floral apex(Fig. 13e, f). The two episepalous stamen primordia keep theupper and lower corolla primordia apart. As the lips enlarge,they fuse at their base and a short corolla tube is formed as inCalceolaria and Jovellana. The slightly smaller median stamenprimordium separates the two lower corolla lobes. Antherdifferentiation of the median stamen lags behind (Fig. 13e–g).

In S. triandra, we have observed two teratological floralbuds that lack a median stamen. In the first bud, anunderdeveloped third stamen primordium was discernible,

Fig. 8. SEM of Jovellana sinclairii, calyx initiation and development. (a) Flower primordium. (b–c) Initiation of sepals (s) in adaxial to abaxialsuccession. (d–f) Further development of sepals, emergence of trichomes on outer surface; calyx bending over and closing the floral apex. (g–i) Furthergrowth of trichomes, (i) calyx approaching mature shape. Bars a–h ¼ 100 lm, i ¼ 200 lm.


and two isolated corolla lobes originated at the lower side ofthe flower (Fig. 13h). In the second bud, which was furtherdeveloped, the median stamen was entirely missing. As a result,only one lower corolla lobe with a median constriction wasdeveloped (Fig. 13i).

DISCUSSION

The flowers of Calceolariceae and historical interpreta-tions—Among the three genera, only the curious flowers ofCalceolaria have attracted major attention, and three principalinterpretations have been proposed (Note: When referring topenta-, tetra- and dimery of flowers, this relates mainly to thecalyx and corolla, occasionally includes the androecium, butdoes not allude to the gynoecium, which is consistentlydimerous in the Lamiales).

1. The flower is derived from a pentamerous condition. Inthis hypothesis, the lower calyx lobe (the smallest of the four

and the last initiated) is interpreted as being formed by twocongenitally fused sepals. The upper corolla lip is considered tobe the fusion product of two petals and the lower lip of threepetals. Of the original five stamens, only two (the upper pair)remain. This view stressing the close relation to traditionalScrophulariaceae is supported by the majority of authors (forreferences, see introduction).

Vogel (1974) was the first to recognize the Calceolariaflowers as oil flowers and studied their morphology in greaterdetail. He regarded the appendage bearing the elaiophore as themedian lobe of three congenitally united corolla lobes, but alsopondered the possibility that it could be a fusion product of allthree abaxial corolla lobes. In both alternatives, the lowercorolla lip is regarded as consisting of three petal lobes.Endress (1999) was the first to study the floral development ofa Calceolaria species (C. tripartita) by means of SEM. Hisstatement, ‘‘The three petals of the lower lip and the two of theupper lip are completely united and the individual organs can

Fig. 9. SEM of Jovellana violacea, development of androecium and corolla; sepals removed. (a–c) Initiation and early development of corolla andandroecium; ul¼ upper lip, ll¼ lower lip of corolla, st¼ stamen primordium. (d–f) Growth of corolla lips and formation of short tube. (g–h) Enlargementof corolla; lips overarching floral apex. (h–i) Emergence of glandular trichomes on their outer surface. Bars a–g ¼ 50 lm, h–i ¼ 200 lm.


no longer be distinguished’’ (p. S15), conforms with thepentamery hypothesis. However, he also admitted thepossibility of tetramery or dimery. Most recently, Sersic(2004) presented a brilliant study of the pollination ofCalceolaria. She provided a floral diagram (reproduced inFig. 14a) showing a tetramerous calyx (said to be derived frompentamery by fusion of the lower sepals, p. 7) anda pentamerous corolla.

2. The Calceolaria flower is tetramerous. Schumann (1890)was probably the first to question the presence of a principallyfive-merous calyx and corolla in Calceolaria. Based ondevelopmental observations, he stated that there was noempirical evidence for a second abaxial calyx lobe and criticizedEichler’s idea of a uniform floral organization of Scrophular-iaceae. In a study of the floral anatomy of C. pinnata, Varghese(1967) described the calyx as truly tetramerous and, based onvascularization, regarded the corolla as composed of four petals.His diagram is reproduced in Fig. 14b.

3. The Calceolaria flower is based on dimery. Thispossibility was recently mentioned by Endress (1999). Indeed,from a formal, numerical point of view, the flower could wellbe composed of two pairs of sepals, one pair of petals, one pairof stamens, and one pair of carpels. Endress, however, did notdiscuss this interpretation in detail, and left open the questionabout pentamery, tetramery, and dimery.

Many descriptions of the Calceolaria flower abstain tacitlyor explicitly from an interpretation. Bentham (1846, 1876),Correns (1891), Ritterbusch (1976), Molau (1978, 1988),

Ehrhart (2000), and others described the calyx simply as four-parted and the corolla as two-lipped, without referring to theirproblematic homology.

The flowers of Jovellana have received much less attentionand those of Stemotria have mostly been misinterpreted. Adiscussion, therefore, can be put aside.

Refutation of pentamery—The results of the present studyand the critical evaluation of literature data make a derivationfrom a pentamerous structure unlikely. There are three maincounter-arguments:

1. The available developmental data (Schumann, 1890;Endress, 1999; this study) give no support for the hypothesisthat the calyx of Calceolariaceae is derived from a pentamerouscalyx. The abaxial calyx lobe is always initiated as a singleprimordium. This is in agreement with the fact that none of thethree genera and none of the numerous Calceolaria species hasa five-merous calyx; it is consistently tetramerous (see Molau,1978, 1988; Ehrhart, 2000; Sersic, 2004). Teratological flowerswith five sepals have been described, but in view of the widerange of reported flower anomalies (described in the nextcounter-argument) evidence from teratology is ambiguous.

2. No evidence is found that the two-lipped corolla iscomposed of five petals. Three arguments in particular in favorof corolla pentamery need to be discussed. (a) The lower lip isoften terminated by three lobes, with the median lobe bearingthe elaiophore and folding inward (Vogel, 1974), thusindicating the presence of three petal lobes. Apart from the

Fig. 10. SEM of Jovellana violacea, stamen and corolla differentiation; floral buds in side view; sepals removed. (a–d) Formation of corolla tube (ct),enlargement of upper (ul) and lower corolla lip (ll). (e–f) Corolla closing over developing inner floral organs, (f–g) emergence of glandular trichomes. Bars¼ 50 lm.


fact that some Calcecolaria species do not produce anelaiophore and a median lobe (18% of the species, accordingto Sersic, 2004), this differentiation is an extremely late eventin development. The three lobes do not result from individualprimordia, but the lower lip is initiated as a single meristematicridge. Like the upper lip, this occasionally has some bipartition(especially Jovellana), but never a tripartition. (b) Stemotriahas a smaller two-lobed upper lip and larger lower lip. Thisstatement is simply based on an incorrect (upside-down)orientation for the flower. It must also be added thatteratological flowers of Calceolaria, with divided corolla lipsand a third stamen, had a similar structure. (c) Teratologicalflowers are pentamerous. In Calceolaria, teratologies such assynanthia (monstrous unions of two or more flowers), pelorias,additional stamens, petaloid stamens have been reportedrepeatedly (Luersson, 1882; Masters, 1886; Anonymus, 1874;Muth, 1899; Penzig, 1921; Sersic, 2004). Of particular interestare pelorias, which are often considered to reflect ancestralforms in alliances with zygomorphic flowers. Indeed, Masters

(1886) and Muth (1899) did so when describing and illustratingpeloric flowers of Calceolaria species and Jovellana punctata(as Calceolaria punctata) with a pentamerous calyx. Sersic(2004) presented a photograph of a flower of C. arachnoideawith a three-lobed lower corolla lip having an elaiophore oneach lobe. However, surveying the pelorias and floralanomalies observed so far, pentamery is only one of thenumerous variations, and practically any theory of floral origincan be supported by Calceolaria teratologies. In fact, thepelorias of Calceolaria appear to be always terminal. As Hartl(1965–1974) pointed out for Digitalis, a terminal peloria (inindeterminate inflorescences) must not be interpreted as singleflowers showing an atavistic regular floral symmetry, but are infact synanthia originating from the fusion of several sub-terminal flower primordia.

3. In Calceolaria and Jovellana, no staminodia are present(or can be detected as vestigial primordia in early development;organ suppression, see Tucker, 1988), which could beinterpreted as remnants of an originally pentamerous androe-

Fig. 11. Stemotria triandra, reproduced illustrations of flowers. From Cavanilles (1799): (a) Habit. (a’) Corolla with similar upper and lower lips,median stamen in adaxial position. (a") Calyx. From Kranzlin (1907): (b) Habit. (b’) Corolla trimerous, upper lip two-lobed, lower lip entire, medianstamen in adaxial position. (b") Calyx and gynoecium. From Molau (1988): (c, c’) Flowers with entire upper and biparted lower corolla lip and medianstamen in lower median position. Bars ¼ 1 cm.


cium. In contrast, the truly pentamerous flowers of Lamialesoften produce staminodia when fertile stamens are reduced.This is frequently the case in the Gesneriaceae (Endress, 1998;Weber, 2004) and varies to a considerable extent in otherfamilies. In Scrophulariaceae s.l., the upper (¼median, ‘‘odd’’)staminode is often very prominent and of functionalsignificance (Penstemon, Scrophularia), but may be reducedor completely aborted in other cases. Complete loss of threestamens is rare and mainly found in the tribe Veroniceae. Here,however, the morphology of the whole flower is different(described in Tetramery in Scrophulariaceae). Still moreincompatible is the situation when the third stamen ofStemotria (and of teratological Calceolaria) flowers isconsidered. This stamen occurs in median-lower (abaxial)position and not in median-upper (adaxial) position. Sucha position is unparalleled in pentamerous flowers of Lamiales.

Tetramery (or dimery?)—The refutation of pentameryseems to lead automatically to the adoption of tetramery ofthe flower. The situation is, however, not that easy. The calyxis the only floral whorl in which tetramery seems to be obvious.The corolla and the androecium, however, consist of twoelements each: two lips and two stamens. The present results(see also Ritterbusch, 1976; Endress, 1999) show that thecorolla lips emerge as two transverse meristematic ridges andnot in the form of four separate primordia that subsequentlyfuse. In Calceolaria and Jovellana, there are only two lateralstamen primordia and no vestiges of a median pair. So the ideathat the flowers are composed of whorls of two (two sepalwhorls and single petal, stamen and carpel whorls in decussatearrangement) appears tempting.

There are, however, arguments against this conception.1. The sepals are not initiated in two opposite pairs. The

observed sequence of initiation can be easily perceived asa unidirectional initiation of a single organ whorl, apparentlycaused by changes of floral symmetry (see Tucker, 1984a, b,1989a, 1999; Endress, 1998, 1999).

2. Though the corolla lips do not result from the pairwisefusion of four petal primordia, a slight central emargination ofthe lip primordia can be often observed (see also Endress,1999: Fig. 5i, j). This is particularly obvious in Jovellana(observed in all three species studied), though the lips of themature flower appear more or less entire. Obviously, we areconfronted here with ‘‘common primordia’’ in which fusion ofprimordia takes place so early that the ancestrally separateinitiation can no longer be observed during ontogeny (see, e.g.,Tucker, 1975, 1981, 1989b; Gerrath and Posluzny, 1988;Kirchoff, 1983; Tucker et. al., 1993; Endress, 1994; Caris andSmets, 2004).

3. Each of the corolla lips receives two lateral vascularbundles, and no median trace is present in either lip (Varghese,1967).

4. Flowers with three stamens (Stemotria, teratologicalCalceolaria flowers) have a deeply incised or emarginate lowerlip. There seems to be a correlation of stamen presence andsplit of the corolla lip. With abortion of the stamen, the split ofthe lip also disappears. The intimate connection of petals andstamens of C. tripartita (and other ‘‘Tubiflorae’’) has beenstressed by Ritterbusch (1976), for which he coined the termstamen-petalum complex (‘‘stapet’’). The two organs form anintimate unity, and reduction of the one obviously influencesstrongly the other.

5. Photographs of Stemotria triandra taken by A. Schmidt-

Lebuhn (Gottingen) from plants in the wild and in cultivationshowed some anomalous flowers, having a tetramerous corollawith a two-parted upper and a similar lower lip. This anomalymight well represent an atavism based on the original tetrameryof the flowers.

Tetramery in Scrophulariaceae—Though members of theScrophulariaceae have fundamentally pentamerous flowers,tetramery is well known in a major group: the tribe Veroniceae.With regard to organ numbers (sepals, petals, stamens, carpels)and the lack of staminodia, their flowers relate well to those ofthe Calceolaria alliance. The similarity, however, is onlysuperficial. There is ample literature dealing with themorphology and development of the flower of Veroniceaeand particular taxa (e.g., Duvau, 1826; Payer, 1857; Noll, 1883;Juel, 1891; Muth, 1899; Lehmann, 1918; J. Fischer, 1920;Saunders, 1934; Yamazaki, 1957; Hartl, 1965–1974; Hong,1984; Lepper, 1984; Hufford, 1992, 1995; Garnock-Jones,1993; Kampny et al., 1993, 1994; Kampny, 1995; Kampny andDengler, 1997; Fischer, 2004), paralleled by recent molecularstudies (see Albach et al., 2004a, b, 2005, and referencestherein). The following statements are generally accepted:

1. In Veroniceae, the widespread tetramery of the calyx isdue to reduction of the uppermost (median) sepal. Allconceivable transitions from a normal presence to diminutionto complete loss are represented, leaving no doubt that calyxtetramery in particular species or genera is a phylogeneticallyderived condition. As always, the uppermost sepal is reducedand the four remaining are placed in a diagonal position, whilethose of Calceolariaceae are arranged orthogonally.

2. The undivided upper lobe of the flower of the coreVeroniceae (Veronicastrum, Veronica, Hebe, and allies,Derwentia and Synthyris) is made up of two fused petals andthus corresponds to the upper lip of other Scrophulariaceae,

Fig. 12. Illustrations of Stemotria triandra, section from a pair-flowered cyme, showing the terminal (T) and the front-flower (F) ofa cyme unit in equal orientation, upper corolla lip (ul) entire, lower lip (ll)two-parted, note third (basal) stamen in superposition to the lower calyxlobe. Drawn after photographs taken by U. Molau, Gothenburg, Sweden.Bar ¼ 1 cm.


while the two lateral lobes together with the lower loberepresent the lower lip. Evidence is derived from thecomparison with related genera (Wulfenia, Picrorhiza, andNeopicrorhiza, with a bilobed upper lobe, Paederota with aneither one- or bipartite upper lobe), vascularization (upper lobeoften with two ‘‘midribs’’ and symmetrical bundle arrange-ment), and teratology (flowers often completely five-merous).Regarding development, however, it must be noted that in(all?) Veronica species the upper lobe is initiated as a single(‘‘common’’) primordium. Nonetheless, no author has takenthis as an indication for true tetramery of the corolla. Twoseparate primordia or an emarginate meristematic ridge mayoccur in Paederota, but data are lacking so far.

The four corolla lobes of typical Veroniceae are thusarranged in an orthogonal cross, while they are in diagonalposition in Calceolariaceae.

3. Though typical Veroniceae have two stamens and lackstaminodia, there are ancestral genera with four stamens(Picrorhiza, Neopicrorhiza).

In summary, the flower of Veroniceae can be well derived

from the pentamerous structure of other Scrophulariaceae, andits structure differs strongly from that of Calceoariaceae. Aphylogentic relationship of the two groups, therefore, cannot beassumed and, in fact, has never been taken into seriousconsideration.

Tetramery in Lamiales—Within the Lamiales, only twofamilies are characterized by flowers with an almostexclusively tetramerous perianth: Oleaceae and Tetrachondra-ceae. The morphology and floral development of these familieswas investigated in a parallel study by E. Sehr and A. Weber(University of Vienna; unpublished data). The flowers of bothare radially symmetric (at least as far as the perianth isconcerned), but differ in the position of the sepals and petalsand the number of stamens. In the Tetrachondraceae (twogenera, three species), the sepals are initiated in diagonal andthe petals in orthogonal position, and four stamens are present.In the Oleaceae, the sepals are initiated in orthogonal positionand the petals in diagonal position (except Nyctanthes andJasminum, in which the arrangement is somewhat irregular due

Fig. 13. SEM micrographs of Stemotria triandra, floral development and teratologies. (a–c) Initiation of sepals (s) in adaxial to abaxial succession;emergence of trichomes on outer surface. (d–e) Same floral buds, with calyx (d) partly or (e–f) entirely removed; initiation of corolla and androecium. (g)Floral bud approaching maturity; calyx distorted due to herbarization. (h–i) Teratologic buds with missing median stamen. All figures oriented with adaxialsepal primordium above. Bars: a–f, h–i ¼ 100 lm; g ¼ 500 lm.


to the five- to eight-mery of the flowers) and usually only twostamens (in transversal position) are formed. The flowers ofOleaceae thus agree remarkably with those of Calceolaria andJovellana. One could even say that the flowers of these generaare oleaceous flowers strongly overformed by zygomorphy.Apart from the unidirectional development of the calyx,a major difference is the presence of four separate petalprimordia in Oleaceae. The occurrence of four stamens inOleaceae has been reported for several genera (Weber, 1928;Melchior, 1964; Wallander and Albert, 2000; Green, 2004).However, all belong to tribe Oleae and thus to a ratheradvanced group of the family (Wallander and Albert, 2000). Itis, therefore, uncertain whether this can be regarded as anancestral condition or a secondary (re-)acquisition. No data arepresently available on whether the median stamen pair isinitiated synchronously or later than the lateral pair.

When speaking of flower tetramery in Oleaceae, Tetrachon-draceae, and Calceolariaceae, this only refers to the conditionobserved in the extant members of these families and saysnothing about the origin and the ancestral condition. In fact,arguments have been proposed that the oleaceous flower isbased on dimery (Torgard, 1924; Weber, 1928). However, nosupport has been found in our developmental studies (E. Sehrand A. Weber, unpublished data). It is also hardly conceivablethat the undivided corolla lips of Calceolaria and Jovellanarepresent a more ancestral condition than found in Oleaceae.

Position of Calceolariaceae in the Lamiales—Even froma strictly morphological point of view, a placement of theCalceolaria alliance within Scrophulariaceae appears no longertenable. An inclusion into Gesneriaceae, with which Calceolar-iaceae share the peculiar type of thyrsic inflorescences withpair-flowered cymes (Weber,1973, 1982; Andersson andMolau, 1980) and similar seeds (aulacospermous, endothelialcells in longitudinal rows and causing longitudinal furrows inthe ripe endosperm; Hartl [1965–1974]; A. Weber, personalobservations) can also be ruled out because of principalpentamery of the Gesneriaceae flowers (Weber, 2004). Theonly sound association is with Oleaceae and Tetrachondraceae,and this is exactly what molecular systematics indicates:Oleaceae represent one of the basalmost families of Lamiales,only preceded by Plocospermataceae and (possibly) Carle-manniaceae, and followed by Tetrachondraceae and Calceolar-iaceae. Peltanthera, Sanango, and Gesneriaceae then forma group with pentamerous flowers and are sister to the ‘‘higher’’Lamiales, which comprise the Scrophulariaceae, Plantagina-

ceae, Stilbaceae, Bignoniaceae, Acanthaceae, etc. (Oxelman etal., 1999; Savolainen et al., 2000; Albach et al., 2001; Bremeret al., 2001, 2002; Olmstead et al., 2001; Andersson, 2003).The molecular evidence thus can be well paralleled andsubstantiated by floral morphology and development. This isconsidered a significant prerequisite for a future multidisci-plinary character evaluation and cladistic analysis of the basalfamilies of Lamiales in order to assess their phylogeneticrelationships more accurately.

Relation between Calceolaria, Jovellana, and Stemotria—From the viewpoint of floral morphology, the three genera arewell characterized and taxonomically separable. Jovellana andCalceolaria indeed placed as sister groups in the molecularstudy of Andersson (2003). As indicated by floral morphology,Jovellana is definitely more primitive than Calceolaria (simplestructure of the corolla lips, lack of an elaiophore). One wouldexpect the same for Stemotria (simple corolla structure, thethird stamen being possibly an atavism). In the molecular tree,however, this genus proved to nest in Calceolaria. Thisunexpected result needs confirmation. Nonetheless, in view ofthe developmental similarity of Stemotria with three-staminateteratological flowers of Calceolaria, the idea that Stemotria(comprising only a single species with narrow distribution) isonly a genetically fixed teratology of Calceolaria, does notseem absurd.

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Calceolariaceae: floral development and systematic implications

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