Note: This paper represents an unpublished manuscript and it should not be cited.
NOLANACEAE
M. O. DILLON
Nolanaceae
Dumortier
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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