Note: This paper represents an unpublished manuscript and it should not be cited.
M. O. DILLON , Department of Botany,
The Field Museum, Chicago, IL 60605, USA.
, Department of Botany, The Field Museum, Chicago, IL 60605, USA.
Annual to perennial, taprooted herbs, or subshrubs to shrubs. Stems erect to ascending, prostrate or procumbent, growth rings present, glabrous to pubescent. Leaves rosulate and/or cauline, alternate or subopposite to fasciculate, simple; petiolate or sessile, exstipulate; blades entire, succulent, dorsiventral, ovate to linear or spathulate, occasionally the bases obliquely decurrent on stems, or greatly reduced, lamina linear, terete, densely pubescent with simple to stellate or branched trichomes, sometimes with apical glands, occasionally with abundant salt glands. Flowers typically solitary in leaf axils or, more rarely, in racemose inflorescenses on modified ascending branches with subtending orbicular floral bracts. Flowers hermaphrodite, actinomorphic to zygomorphic, the floral asymmetry involving perianth and the androecium or only the androecium; 5-merous. Sepals 5, 1-whorled; fused, equal to unequal, regular to sub-bilabiate, rarely reduced to an unlobed truncate tube, persistent, enclosing the fruit; imbricate or valvate. Petals 5, corolla gamopetalous, plicate between lobes; infundibuliform, campanulate or tubular, more rarely sub-urceolate or salveriform; regular or sub-bilabiate; blue, purple, lavender or white, the limb basally dark purple or white, with or without pale yellow, white or green bands. Stamens 5, filaments adnate basally, often pubescent, unequal (3 long, 2 short), antisepalous, anthers dehiscing via longitudinal slits, introrse. Pollen shed as single grains, 3-colporate. Hypogynous disc annular, crenate or lobulate, nectar secreting. Gynoecium fundamentally 5-carpellate; in subg. Aloa the carpels are united to form a superior, (3-)5(-6) locular ovary with a terminal style and basal-axial placentation which develops into a dry fruit of (3-)5(-6) several-seeded mericarps; in subg. Nolana the carpels are strongly lobed with each lobe normally containing one ovule; the style is gynobasic and the ovary develops into a dry fruit of up to 30 normally one-seeded mericarps.) Stigma capitate or peltate, wet. Cotyledons 2. Embryo curved or coiled. Chromosome number: x = 12.
~84 species, coastal Chile and Peru and one species confined to the Galápagos Islands.
VEGETATIVE MORPHOLOGY AND ANATOMY. Nolana species can be considered essentially herbaceous with woodiness varying from nearly absent in annuals to moderate in shrubs (Carlquist, 1987). The geographic distribution of woodiness suggests that the greatest concentration of shrubs is in northern Chile and the greatest concentration of annuals is in southern Peru. Many species are facultative annuals, only discontinuing growth due to an absence of available moisture. If allowed to mature with a continuing supply of water, some rosette-forming species form a central stem that elongates and leads to another rosette of leaves. With sufficient moisture, some species form much-branched mats several meters in diameter.
Carlquist (1987) reviewed the wood anatomy of six Nolana species and found that all essential characters, with the exception of terminal parenchyma, were common to the Solanaceae, i.e., growth rings present, vessels with simple perforation plates; lateral wall pitting of vessels composed of alternate circular pits with narrowly elliptical apertures; imperforate tracheary elements either fiber-tracheids with vestigial borders on pits or libriform fibers; vasicentric tracheids and axial parenchyma present, but tangential bands of axial parenchyma present; ray cells predominantly erect, square and erect; wood non-storied. Carlquist (1987) suggested that the wood anatomy was indicative of paedomorphosis. Crystal sand has been observed in the wood of Nolana and some Solanaceae.
Most Nolana species display some degree of leaf succulence. The leaf shape is highly variable but usually lanceolate to linear or spherical and terete. Leaf reduction to 1--5 mm long and 1 mm wide is most pronounced in shrubby species. The largest leaves are found in Nolana rupicola with ovate to lanceolate leaf blades up to 15 cm long and 10 cm wide.
Several different types of foliar trichomes are present, including dendritic to stellate trichomes, unbranched, non-glandular trichomes, glandular-capitate trichomes, and salt glands. All these trichomes types have been reported previously from the Solanaceae (Haegi, 1991). The quantity of pubescence is variable and ranges from essentially glabrous to densely canescent. Species with salt glands exude salt onto the surface of their leaves; this salt has been shown to be effective in condensing moisture from an unsaturated atmosphere (Mooney et al., 1980).
INFLORESCENCES. Most commonly, flowers are solitary in leaf axils. Flowering may occur in the earliest developmental phase when the plant has reached only a few centimeters in height. Usually stems are unmodified and flowers are borne along the branches, but in a few species, modified branches arise from a basal rosette, and these form racemose inflorescences with reduced, subtending floral bracts.
FLORAL MORPHOLOGY. Floral anatomy and development have been studied in only a few species (Armstrong, 1986; Bruno, 1994; Bondeson, 1986; Di Fulvio, 1969, Huber, 1980). Nolana has pentamerous flowers with distinct calyx and corolla. Sepal lobes are equal to subequal in length and may be free apically or unequally fused. Corollas are regular, or more commonly irregular to weakly zygomorphic, with primary modifications in the size, shape and coloration patterns. The most common color is lavender to blue, with considerable variation in the bands of colors or colored veins within the throats; white forms are observed at a low frequency in some species. The five fertile stamens have filaments unequal in length (i.e., 2 short, 3 long) and are adnate to the base of the corolla and often pubescent.
The development of the carpels is unique in the subdivision of the loculi into locelli (Bondeson, 1986). Subg. Alona has (3-)5(-6) sulcate, multi-seeded mericarps broadly affixed to the receptacle. The ovules are located in uniovulate depressions of the adaxial carpel wall. In subg. Nolana these uniovulate depressions develop into normally one-ovulate lobes. The style is either apical (subgenus Alona) or gynobasic (subgenus Nolana).)
In the Solanaceae, the ovary is predominantly a 2-carpelled gynoecium and this difference has led workers to treat Nolana as a separate family, Nolanaceae (Bondeson, 1986; Cronquist, 1981; Johnston, 1936; Mesa, 1986; Saunders, 1936). It is noteworthy that Nicandra physalodes (L.) Gaertner, clearly a member of the Solanaceae but not closely related to Nolana, contains an obviously 5-carpelled gynoecium (Huber, 1980).
EMBRYOLOGY. Two species have been investigated (Datta, 1936; Di Fulvo, 1969). Embryo sac development was characterized as the Polygonum-type and endosperm formation is cellular, haustoria absent, similar to that found in the Solanaceae.
POLLEN MORPHOLOGY. Pollen is tricolporate, blue or white and comparable to that found in the Solanaceae (Di Fulvo, 1969; Mesa, 1981) and specifically the Solaneae (Solaninae fide Murry & Eshbaugh, 1971). Shapes range from subprolate or prolate spheroidal to oblate spheroidal; the exine is tectate; the ektexine is thicker than the endexine, striate to striate-reticulate.
KARYOLOGY. Chromosome counts reported for Nolana suggest the base chromosome number to be x = 12 with 2n=24 reported from the following species: N. galapagensis (Eliasson, 1970), N. humifusa (Datta, 1933), N. paradoxa (Datta, 1933; Di Fulvio, 1969), and N. rostrata (Di Fulvio, 1984).
POLLINATION. No published accounts of Nolana pollinators are available. However, from field observations, it appears that most species are generalists and visited by beetles, butterflies, moths, flies, ants, and wasps. One Coleoptera genus, Epicante, feeds exclusively on Nolana corollas and may complete pollination. The presence of abundant Thripidae in the corollas of several species suggests that they may be reservoirs or alternative hosts for agricultural pests.
REPRODUCTIVE SYSTEMS. Darwin (1877, p. 261) commented on the individual variability of pistils in Nolana, and suggested that the condition was a step towards heterostyly. Heterostyly was reported in Nolana by Mesa (1981) and many species exhibit some degree of style-stamen polymorphism accompanied by polymorphisms in the color and size of pollen. Detailed studies are needed to confirm that the variability demonstrated in Nolana is true heterostyly.
FRUIT AND SEED. There are either (3-)5(-6), several-seeded (subg. Alona) or up to 15 normally one-seeded (subg. Nolana) dry mericarps. The mericarps are only attached to the receptacle and essentially free from one another. In a few species, mericarp number is reduced to 2 or 3 through abortion (subg. Alona) or increased to as many as 30 (subg. Nolana). Mericarp shape is highly variable from polygons to spheres and external sculpturing smooth to rugulose. The seeds have copious oily endosperm, ovules are anacampylotropous, unitegmic and tenuinucellate. Germination is phanerocotylar.
DISPERSAL. Mericarp dispersal is essentially passive, with the persistent accrescent calyx containing the detached mericarps; however, transport by birds or small mammals cannot be ruled out. Mericarps have been found in underground rodent middens in northern Chile (Betancourt et al., 2000). The rounded mericarps in some species may be dispersed by wind or water. In a few species, the mericarps are flattened with edges narrowed into wings that may play a role in dispersal. In one annual species from dune habitats, the branches bend inward during senescence, curling into a sphere with the characteristics of a tumbleweed, unrooting and rolling over the dunes.
PHYSIOLOGY. Nolana species are often succulent and photosynthesis has been investigated in a few (Ehleringer et al., 1998; Tago, 1999). Tago (1999) reported finding carbon isotope ratios generally accepted as within the range of CAM plants in various Chilean species; all Peruvian species investigated had ratios representative of C3 photosynthesis. Ehleringer et al. (1998) suggested that these values are not conclusive evidence for CAM. The Nolana species analyzed thus far suggest high water use efficiency, but perhaps not CAM photosynthesis. Neither C4 nor CAM plants have been reported previously for the Solanaceae (Smith & Winter, 1996).
PHYTOCHEMISTRY. Bate-Smith (1962) reported the occurrence of hydroxyflavonols, quercetin and kaempferol, compounds also known in the Solanaceae. Chamy et al. (1997) and Garbarino et al. (1986, 1988) reported the occurrence of diterpenoids, and Garbarino et al. (1993) reported the occurrence of sesquiterpenoids. No cyanogenic compounds, iridoids, ellagic acide or proanthocyanidins have been reported.
RELATIONSHIPS and SYSTEMATICS. The Nolanaceae was proposed by Dumortier (1829) and accepted as a distinct family (Cronquist, 1981; Mesa, 1986) or at subfamilial rank within the Solanaceae (Dahlgren, 1980; D’Arcy, 1979, 1991; Takhtajan, 1980; Thorne, 1968, 1983, 2000). D’Arcy’s (1991) recognized 22 species in two genera, Alona and Nolana in the tribe Nolaneae (Solanoideae).
Olmstead et al. (1999) presented phylogenetic analyses of the Solanaceae based on restriction site variation of the entire chloroplast genome (Olmstead & Palmer, 1992) and DNA sequences of two genes, rbcL and ndhF (Olmstead et al. 1992, 1994; Olmstead & Sweere, 1994). These analyses contained one species of Nolana, and Nolana was deeply nested within the Solanaceae-Solanoideae in a clade with Lycium and Grabowskia (Lycieae). Johnston (1936), on morphological evidence, already had suggested that Nolana shared relationships with both Lycium and Grabowskia. When incorporated in the Solanaceae, Nolana becomes the fifth largest genus of that family (D’Arcy, 1991).
The early taxonomic history of Nolana was reviewed by Johnston (1936) and Mesa (1981). Dunal (1852) recognized 33 species in five genera, Nolana L.f., Dolia Lindl., Alibrexia Miers, Aplocarya Lindley, and Bargemontia Gaud. in the tribe Nolaneae of Solanaceae. Bentham and Hooker (1873) recognized 27 species in four genera, Alona, Nolana, Dolia, and Bargemontia, in tribe Nolaneae of Convolvulaceae. Johnston (1936) provided the first modern monograph treating 63 species.
Mesa (1981, 1989) interpreted the group narrowly, accepting only 18 species in a single genus, Nolana, with two sections, Nolana sect. Alona (Lindl.) Miers with five species and Nolana sect. Nolana with 13 species in two subsections, subsect. Bargemontia (Gaud.) Mesa (7 spp.) and subsect. Nolana (6 spp.). The vast majority of the named species were reduced to synonymy. Recently, Mesa (1997; et al., 1998) has expanded his species concepts to accept 70 species. Tago and Dillon (1999) recognized a total of 83 species in a single genus, Nolana, with two subgenera, Alona and Nolana
Tago (1999) analyzed sequence data in 37 species of Nolana for both ITS and matK . Results (Tago, 1999; Tago & Dillon, 1999) provided conflicting hypotheses of relationships in Nolana; however, the genus was clearly monophyletic and there was weak support for at least two subgenera, Alona and Nolana.
Tago (1999) calculated the divergence time of Nolana from Grabowskia at ~11.6 million years ago using ITS and ~11.0 million years ago for matK. Using comparative rbcL, Olmstead and Palmer (1992) estimated the origin, or at least early diversification of the Solanaceae to be ca. 50 million years ago and the first appearance of Nolana at ~10.6 million years ago or less.
DISTRIBUTION AND HABITATS. The ecological preferences of Nolana are essentially arid and semi-arid habitats throughout the Atacama and Peruvian deserts (Dillon, 1997; Dillon & Hoffmann 1997). The greatest concentration of species is in near-ocean localities between 50--600 meters elevation and within a few kilometers of the shoreline, and habitats range from highly saline beach dunes to inland and/or upland habitats (Rundel et al., 1991). Some Chilean species grow in habitats termed aguadas that are moist areas fed by underground water in dry quebradas, typically highly saline or alkaline.
Most species are narrow endemics, with small, restricted geographic ranges and specific ecological requirements. Nolana galapagensis is restricted to sandy dunes near the ocean on four islands within the Galápagos Island chain (Wiggins & Porter, 1971). A few species have wide distributions or occur over wide altitude ranges. Nolana species are often important members of their respective communities.
ECONOMIC IMPORTANCE. Only two species, Nolana paradoxa (“Bluebird” and “Snowbird”) and N. humifusa (referred to as “N. prostrata”) have found their way into the horticultural trade. Artificial hybrids between these two species yielded Nolana tenella Lindl., that may still be found in cultivation (Johnston, 1936).
Only one genus:
Nolana Linnaeus f., Decas Prima Pl. Rar. Horti. Upsal. t.2 (1762)
~Alona Lindley, Edwards’s Bot. Reg. 30:: ad t. 46 (1844)
Description as for the family. Two subgenera (Tago & Dillon, 2000) or genera (D’Arcy, 1991) have been proposed.
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