Calyceraceae

Calyceraceae R. Br. ex Rich., Mem. Mus. Hist. Nat. 6: 74 (1820), nom. cons. F.H. Hellwig

Perennial or rarely annual herbs, occasionally subligneous, often stemless or with scapiform flowering shoots. Leaves alternate, often forming a basal rosette, somewhat fleshy, without stipules, sessile or narrowed into a distinct petiole, undivided to dissected, margin entire, sinuate, dentate or serrate, sometimes revolute. Flowers in capitula, surrounded by triangular to lanceolate involucral bracts which are more or less united. Receptacle flat to conical, often with herbaceous to membranous, subulate to obovate or lanceolate receptacular bracts, usually free but rarely fused. Flowers perfect or rarely functionally male (and then plants andromonoecious), epigynous, acti-nomorphic, calyx adnate to the ovary, with (4)5(6) small, hyaline to membranous lobes or teeth, these rounded-orbicular or flat, linear-lanceolate and tapering. Corolla sympetalous, pentamerous or sometimes tetramerous, only occasionally hexamerous in individual flowers, cylindrical to narrowly infundibuliform with (4)5 short corolla lobes or with a slender basal tube and a widened limb, uppermost part campanulate with (4)5 valvate lobes, white or greenish. Stamens enclosed in corolla or subexserted, (4)5(6), as many as and alternating with the corolla lobes, inserted at various levels in the corolla. Filaments united into a tube over most of their length, sometimes distally free; anthers connate, at least at their bases, tetrasporangiate, dithecal, introrse, opening by longitudinal slits, mostly without appendages, sometimes with subsagittate bases and inconspicuous apical appendages. Nectary glands at base of filament tube alternating with the vascular bundles of the filaments. Gynoecium of two carpels, unilocular, inferior. Ovule solitary, pendulous, anatropous, tenuinucellate. Style strongly exserted, slender, cylindrical, stigma capitate, dry, papillose, with two (three) vascular bundles. Fruit an achene, often crowned by the calyx lobes which sometimes become lignified and spiny, often calyx also accrescent; achene cylindrical or prismatic, more or less distinctly ribbed. Seed with well-developed endosperm, embryo straight.

The family comprises four genera and about 60 species and is endemic to southern South America. One species occurs in the Falkland Islands (Islas Malvinas).

Vegetative Morphology. Besides inconspicuous annual herbs, the family contains many species which form vegetative rosettes until the inflorescences are formed. Growth is then continued by stolons, rhizomes or by lateral shoots arising from lower parts of the plant. Branching of Calyceraceae is sympodial, and in some genera monochasia are formed (in Acicarpha the capitula are terminal and the shoot system is continued by secondary axes overtopping the preceding ones). Metatopies with re- and concaulescence can be observed in some species (e.g. Calycera sessiliflora, C. eryngioides).

Vegetative Anatomy. Plants usually are glabrous but sometimes uniseriate filiform hairs are present, especially on the stems (Calycera). No external glands or secretory cavities have been observed (Hansen 1992), nor are resin-like droplets present in the wood (Carlquist and DeVore 1998). However, droplets of a resin-like substance seem to be present on and in stems and involucral bracts of Boopis gracilis (pers. obs.). Stem vascular bundles are arranged in a circle and are separated from each other by broad rays. The bundles are embedded in a ring of mechanical tissue in some species (Boopis spp.). Phloem strands of Acicarpha are accompanied externally by sclerenchyma, xylem includes moderately wide vessels with simple perforation plates, with bordered pits between vessels and ray parenchyma. Secondary medullary rays are wanting (Cronquist 1981). Two types of imperforate tracheary elements occur in the family, i.e. vasicentric tracheids and libriform fibres, the latter with small simple pits. Pits between vessels and libriform fibres are alternate and circular to oval (Carlquist and DeVore 1998). Laterally elongated pits, called pseudoscalariform pits, are present in several species of Calyceraceae (Carlquist and DeVore 1998). The amount of wood is always very limited, with a maximum at stem bases and adjacent parts of the roots (Carlquist and DeVore 1998). The wood has strong indications of paedomorphosis with varying degrees in different species. This is supported by the presence of pseudoscalariform pitting and predominantly upright ray cells (Carlquist and DeVore 1998). Secondary xylem vessels with pseudoscalariform pitting transitional to helical-banded patterns support the ability of the roots to be bent or to expand and contract in reaction to changing water content (Boopis graminea, Nastanthus spp.). Seasonality is mirrored in the formation of growth rings observed in Boopis anthemoides (Carlquist and DeVore 1998).

The family exhibits an unusually wide range of mesomorphy values. This may be explicable by the very different habitats the plants live in. Wood anatomy is not yet sufficiently known to be used systematically. It is believed to largely reflect autapomorphic ecological adaptations (Carlquist and DeVore 1998). The primary cortex and the central pith are rich in clustered Ca-oxalate crystals. There are no specialized bast strands in the cortical parenchyma (Reiche 1901). The fleshy stems found in various species of Boopis result from the presence of massive medullary and cortical parenchyma (Reiche 1901). Tuberous roots of the fleshy species of Boopis have a strongly transversely rugose cortex which is a feature connected to the ability of many alpine plants to translocate themselves into deeper strata of the soil by root contraction (Reiche 1901).

Inflorescence and FLower Structure. The most striking feature of many species is the condensed, often many-flowered inflorescence. This condensation reaches several levels in the family. While Acicarpha has simple capitula with centripetal anthesis, the other genera have more complicated capitula of higher orders. It has been hypothesized that these consist of cymose units (Baillon 1880; Reiche 1901; DeVore 1994) but this has not been confirmed by detailed analyses. Some species of Calycera and Boopis tend to aggregate few to many capitula.

Flowers usually are hermaphrodite but functionally male flowers occur regularly in the centre of the capitula of Acicarpha (Miers 1870). The flowers are characterized by the transformed calyx and a close association of corolla, androecium and the style. The free part of the calyx is reduced to five small lobes above the edges of the gynoecium, the lower part being fused and closely attached to the inferior ovary. It does not protect the flower bud (Erbar 1993).

The filaments form a tube which consists of their fused lower parts. In Acicarpha tribuloides, this tube overtops the corolla tube in mature flowers. Below the separation of the filaments from the corolla tube, there is a corolla stamen tube. Five nectaries are present in the flower. The glandular tissue extends from the base of the filament tube to the top of the stamen corolla tube (Erbar 1993). Nectar is secreted through nectar slits outside of the filament tube into five small pockets. Form and alternate position with the filaments of the nectaries are very distinctive for the family (Brown 1817; Reiche 1901). The style is cylindrical with a club-like papillose head. Intercalary growth of the receptacle results in a carpel stamen corolla tube between the ovary and the other parts of the flower, except the sepals. This feature seems to be unique among the families of Asteridae (Erbar 1993). The unilocular gynoecium usually is interpreted to consist of two carpels (Cronquist 1981). Investigations by Erbar (1993) and Hansen (1992), however, revealed the existence of five ledges in the ovary which can be interpreted as rudimentary septa. Following this interpretation, the family has five carpels (Erbar 1993).

FLoraL Anatomy. The free corolla contains 10 parallel longitudinal vascular bundles. The com-missural bundles are bifurcated below the corolla lobes and anastomose with the median bundles of the corolla lobes just below their apex (Gustafsson 1995; Gustafsson and Bremer 1995). Micromorpho-logical characters of the corolla (petal epidermis patterns) are rather uniform in the Calyceraceae, the cells always being Senecioid. Cells are often long (more than 200 pm) and confluent. A transversely striate pattern prevails on the adaxial surface, while the abaxial pattern is mostly longitudinally striate although rugose, reticulate-rugose or glabrous cells also occur. The cells are generally distinctly sculptured on both surfaces (Hansen 1992).

Embryology. An integumentary tapetum is formed by the innermost layers of the one massive integument (Dahlgren 1915). The mature embryo sac has eight nuclei; the polar nuclei fuse before fertilization. The seed, which is suspended from the top of the locule and fixed by a short funiculus near the upper end of the seed, contains a straight, terete embryo and abundant endosperm (Cron-quist 1981). Endosperm development is cellular, and no haustoria are formed. The endosperm contains protein grains, rather than starch. The outer cells of the testa contain chloroplasts before the seed is mature. The radicula points towards the micropyle, i.e. the apex of the seed (Miers 1870). The pollen grains are binucleate when released. No periplasmodial tapetum is formed in the pollen sacs (Dahlgren 1915).

Pollen Morphology. Pollen grains of Calycer-aceae are tricolporate. The colpi are very long, rendering the grains of some species sub-syncolporate. The colpus membrane is more or less granular. The pores are lalongate, the ends overlapping or joined, forming a colpus transversalis of irregular width in some species (Heusser 1971; Markgraf and D'An-toni 1978). Minute spinules are usually present on the pollen surface but rarely they are almost lacking. The exine has thickened ridges above the pores and rounded depressions in the mesocolpi. A granulate colpus margin (Skvarla et al. 1977) is prominent in many species. The pollen grains rarely exceed 30 pm in length and 20 pm in width, and are often rather irregularly shaped. The majority of pollen grains are at first glance spheroidal but, seen in equatorial view, they are irregularly rhomboidal (Hansen 1992). Prolate (elliptic, ellipsoidal) grains occur in a few species. Dimorphic grains are rare (Boopis gracilis) but shape can vary within species. Avetisjan (1980) distinguishes two pollen types in the family, the Moschopsis-type and the Calycera-type. They differ by the shape of pollen grains (polar view rounded, three-lobed, elliptical in equatorial view, pores elliptical in the Moschopsis-type, polar view irregularly hexagonal, equatorial view transversely elliptical, pores broad-elliptical (la-longate) in the Calycera-type) and by the shape of the colpi, especially by the ridges above the apertures, which are weakly to moderately thickened in the Moschopsis-type and strongly developed in the Calycera-type. The Moschopsis-type is regarded as primitive, and the Calycera-type as derived by the author. The pollen grains have TEM-patterns approaching the plesiomorphic Anthemoid pattern of Compositae, i.e. with distinct infratectal bac-ula and an infratectum. The tectum is massive and a cavus is lacking (Hansen 1992).

  1. Several chromosome numbers are known in the family. Stebbins (1977) suggested x = 7, 8 and 9 as base numbers. The only known diploid species of the family is an Acicarpha (DeVore 1994). All other species investigated are interpreted as being polyploid. Accepting this, species of Calycera and the species of Boopis based on x = 7 are mostly hexaploid or hexaploid-derived, or derived from tetraploids, and species of Boopis with the base number x = 9 are tetraploid or tetraploid-derived. In Calycera, n = 21 or 22, 17 and 13 are found in the Chilean species, while Argentinean species are all polyploids with n = 21. DeVore (1994) interprets the base number x = 8 as ancestral; x = 7 would then have originated by descending aneuploidy, and the counts in Boopis point to the other derived base number x = 9. However, the interpretation of karyotype evolution in Calyceraceae is inconclusive, due to lack of data and a well-supported phylogenetic hypothesis.
  2. Calyceraceae show secondary pollen presentation. The mechanism corresponds to the pump mechanism (Leins and Erbar 1990) as known from Acicarpha. This mechanism seems to prevail in some basal lineages of Asteraceae (Bremer 1994). Initially, the pollen grains are released into the cavity of the anther tube which is basally sealed by the tip of the style. The pollen is then extruded apically by the growing style. One major difference to the pump mechanism of Asteraceae is that the anthers are not fused over their entire length in many species, and are bent outwards at least in Acicarpha tribuloides.

Fruit, SEEd ANd SEEd Dispersal. The gynoecium consists basically of two carpels forming a compound, inferior, unilocular, pseu-domonomerous ovary (Cronquist 1981). The fruit is an achene, crowned by the persistent lobes of the calyx. In some species, all lobes or some of them are enlarged and become indurated to spine-like structures. In Calycera, capitula are distinctly heterocarpic. In Calycera eryngioides, the smaller achenes are dispersed individually whereas those with elongated calyx lobes remain attached to the receptacle and are dispersed with the whole capitulum (DeVore 1994). Acicarpha is characterized by partly fused achenes which remain attached to the receptacle. The spine-like elongated calyx lobes point to epizoochorous dispersal. A spongy tissue in the pericarp may facilitate hydrochory or even anemochory.

Phytochemistry. Calyceraceae commonly produce iridoid compounds, e.g. seco-loganin (Jensen et al. 1975), but are not tanniferous. They lack pro-anthocyanins and presumably also ellagic acid. No latex or secretory cavities are known (Cron-quist 1981). The seeds store inulin (Cronquist 1981; Bohm et al. 1995). Acetylenes (Mabry and Bohlmann 1977), sedoheptulose, aluminium accumulation, raphides, leucoanthocyanins, cyanoge-nic glycosides, saponins and l-inositol are absent (Gibbs 1974). For flavonoids, refer to Bohm et al. (1995).

Distribution and Habitats. The family is endemic to southern South America. Its range extends from the extreme south of the continent to southern Peru and Bolivia in the west and as far north as Bahia (Brazil) in the east. One species occurs in the Falkland Islands (Islas Malvinas). Most species grow in high-altitude arid habitats, e.g. open grassland and meadows, in the Andes of Chile and Argentina. A few species grow in coastal sand dunes. Acicarpha tribuloides grew in the south-western United States for some decades in the 19th century after it was introduced by man, but did not become naturalized there (DeVore 1991).

Subdivisions and Relationships in the FamiLy. The generic classification of the family is unsatisfactory. Currently, six genera are widely accepted (Reiche 1901; Pontiroli 1963; Marticorena and Quezada 1985; Chiapella 1999). Possibly apo-morphic characters have been identified for Acicarpha, Calycera and Gamocarpha but not for Nas-tanthus, Boopis andMoschopsis (Hansen 1992), and the diagnostic characters reported for these latter three genera proved to be unsuitable because of erroneous observations and misinterpretations of morphology. In the present treatment, Boopis, Moschopsis and Nastanthus are united under the oldest generic name, Boopis, in order to obtain recognizable genera. The relationships among the genera of the family are discussed in several papers without satisfactory result. The only unanimously accepted fact is that Acicarpha is distinct from the other genera by centripetal anthesis within the capitula and the presence of functionally male flowers in the centre of the receptacle. It is further believed (DeVore 1994) that Calycera and Nastanthus are closely related to each other (chromosome numbers), while the relationships of Boopis, Gamocarpha and Moschopsis remain uncertain (Hansen

1992). No formal phylogeny has been published for the family.

PhyLogeny and Systematic Position of the FamiLy. Calycera herbacea, the first species of Calyceraceae described (Cavanilles 1797), was placed in Dipsacaceae by Ruiz and Pavón in 1798, and the family was kept in Dipsacales by several taxonomists throughout the last two centuries. On the other hand, Acicarpha tribuloides, described by Jussieu in 1803, was included, although with doubts, in Asteraceae by the author. In 1816, Brown and Cassini independently recognized Calyceraceae as a separate family in oral presentations before the Linnaean Society and the French Académie des Sciences respectively, and placed it between Dipsacaceae and Asteraceae (see also Cassini 1817). The nomenclaturally valid publication of Calyceraceae was provided by Richard (1820). Miers (1870) underlined the close affinity between Asteraceae and Calyceraceae. Cladistic studies in Asteridae supported such relationship (Gustafsson 1996). The family is very likely to be the closest living relative ofCompositae (Lundberg and Bremer 2003). This position is indicated not only by evidence from DNA sequence variation but also by characters such as pollen morphology, petal venation, morphology of the receptacle and receptacular bracts, and wood anatomy (DeVore and Stuessy 1995; Carlquist and DeVore 1998). Similarities with Dipsacales include the pendulous ovule, copious endosperm, morphology of capitula in the majority of Calyceraceae, and phytochemical features such as the absence of iridoid compounds from Asteraceae. This may have caused Dahlgren (1989) to place Calyceraceae in Dipsales. However, iridoids are found also in Goodeniaceae, a family closely related to Calyceraceae plus Asteraceae and Menyanthaceae. Lack of iridoids in Asteraceae may therefore be apomorphic for this family. Hansen (1992) and Erbar (1993) provide a summary of differences and similarities of Calyceraceae with various possibly related groups (see also Moore

1993). The molecular phylogenetic studies of Gustafsson and Bremer (1995) and Albach et al. (2001) showed Calyceraceae as sister to Asteraceae, while Calyceraceae are sister to Goodeniaceae in the combined 18S/rbcL analysis of Bremer et al. (2001), as they were in previous rbcL analyses (Cosner et al. 1994; Gustafsson et al. 1996). This latter position is supported by chemical features: both contain bis-secoiridoids of the sylvestroside type (Jensen et al. 1979; Capasso et al. 1996). The combined analysis of morphology, rbcL and ndhF sequences confirmed the sister-group relationship between Calyceraceae and Asteraceae, while Good-eniaceae were placed as sister to these two (Bremer et al. 2001). Takhtajan (1997) established the order Calycerales, which is not recognized in systems which reflect the results of cladistic studies.

Economic Importance. Some species are weeds in South America (Boopis gracilis, Boopis anthe-moides, Acicarpha tribuloides). Medicinal use of Acicarpha tribuloides has been reported (Capasso et al. 1996).

Key to the Genera

1. Capitula with dimorphic flowers, upper/central flowers functionally male, lower/outer flowers hermaphrodite; all achenes with spiny calyx lobes, outer achenes with united bases and also fused to the receptacle 1. Acicarpha

- Capitula with isomorphic flowers, all flowers hermaphrodite and fertile; achenes not united 2

2. Achenes dimorphic, some with spiny calyxlobes, some without 2. Calycera

- Achenes monomorphic, without spiny calyx lobes 3

  1. Receptacular bracts fused into groups, these and involucral bracts around groups of flowers
  2. Gamocarpha

- Receptacular bracts free or absent 4. Boopis

Genera of Calyceraceae 1. Acicarpha Juss.

Annual or perennial herbs; stems more or less branched, erect or procumbent, terminating in an inflorescence overtopped by lateral branches. Leaves petiolate or sessile, subamplexicaulous, undivided to pinnatifid, margin entire to dentate, leaf bases attenuate to auriculate. Capitula solitary, sessile or pedunculate; involucral bracts about five in one series, linear-oblong, unequal, similar to the uppermost cauline leaves, fused in their lower part; receptacle convex to conical; receptacular bracts free, linear to lanceolate. Flowers pentamerous, dimorphic, the outer (or lower) hermaphrodite, the upper (or central) functionally male; corolla with a long slender tube and an infundibuliform to campanulate limb deeply divided into five corolla lobes; stamens 5, enclosed, fused to the lower 2/3 of the corolla; anthers connate from base to middle, free in distal part and bent outwards at anthesis; achenes cylindrical to obconical, pentasulcate to prismatic, crowned by variously elongated spiny calyx lobes. Marginal achenes fused to the receptacle and united with each other. 2n = 16. Three species in Brazil, Peru, Bolivia, Paraguay, Uruguay and Argentina.

2. Calycera Cav.

Annual or perennial herbs, glabrous or weekly lanuginose; stems erect or decumbent. Leaves alternate or in rosettes, undivided to pinnat-ifid, spathulate to elliptical; margin entire to dentate-mucronate. Involucral bracts 4-7 in one series, sometimes with additional bracts, broadly triangular to linear-lanceolate, united to various degrees, entire or dentate; receptacle convex or subglobose; receptacular bracts lanceolate to linear or absent. Flowers hermaphrodite, tetramerous or pentamerous; corolla with a long tubular part and an infundibuliform to campanulate limb, or limb more or less truncate at base, abruptly narrowed into a short slender tube, upper part of limb divided to various degrees into four or five lobes; stamens 4 or 5, not exserted, inserted at the base or higher up in the corolla tube; anthers connate, bases rounded or sagittate, connectives sometimes with apical appendages; achenes cylindrical to obconical or prismatic, dimorphic, some crowned by short or long spiny calyx lobes, some with only very short calyx lobes, not spiny. 2n = 26, 24, 42, 44. About 20 species, Andes of Bolivia, Chile and Argentina. Two subgenera, subg. Calycera and subg. Leucocera (Turcz.) Reiche, have been distinguished (Miers 1870; DeVore 1994).

3. Gamocarpha DC.

Perennial herbs, glabrous, some species stolonif-erous. Leaves generally forming a rosette, entire or divided. Capitula surrounded by 6-12 involu-cral bracts, these and receptacular bracts more or less fused, forming chambers which contain several flowers. Bracts with triangular distal parts, fused in the lower part, entire or weakly lobed. Flowers pen-tamerous (occasionally tetramerous); corolla tube long, slender, with an infundibuliform to campan-ulate limb, corolla lobes long, or corolla cylindrical to infundibuliform, base sometimes abruptly narrowed into a short filiform tube, corolla lobes short; anthers subsagittate at base, connate in the lower part; achenes cylindrical to prismatic, ribs weak, crowned by ovate to triangular non-spinescent calyx lobes. Six or seven species in Chile and Argentina.

Boopis Juss., Ann. Mus. Natl. Hist. Nat. 2: 350 (1803).

Perennial or rarely annual herbs, glabrous; stems erect or decumbent, scapose or ramified. Leaves alternate or clustered in a rosette, entire to pinna-tisect, linear-lanceolate, laciniate, dentate or pectinate, or spathulate with dentate or crenate lamina. Capitula terminal, solitary or in groups of few, then shortly pedunculate to almost sessile, sometimes densely surrounded by foliar leaves, rarely

Ssp Boopis
Fig. 4. Calyceraceae. Boopis bupleuroides. A Habit. B Inflorescence. C Flower bud, longitudinal section. D Open flower. E Fruit. F Fruit, longitudinal section. (Martius 1878)

scapose. Terminal capitula sometimes overtopped by axillary shoots, in some species terminal and lateral scapes forming a disk-like to hemispherical syncephalium; involucral bracts 5-10, united from basis to middle or beyond, exceptionally free, triangular to lanceolate, sometimes laciniate; receptacle flat to convex or conical, inflated in some species; receptacular bracts free, linear to lanceolate, or absent. Flowers pentamerous or tetramerous, hermaphrodite, uniform within species; corolla with short or moderately long tube and cylindrical to infundibuliform or slightly campanulate limb, or with slender tube and limb consisting of lower infundibuliform part and distal, more or less campanulate part; corolla lobes mostly short, long in flowers with long tube; stamens five or four, anthers connate at their base, free in the upper half; achenes prismatic, 5- or 4-ribbed, ribs crowned by ovate or broadly lanceolate, acute, more or less rigid but not spiny calyx lobes. 2n = 36, 40, 42. About 30 species, some of them polymorphic, in Chile, Argentina incl. Islas Malvinas (Falkland Islands), very few in Brazil, Peru, Bolivia.

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