The Genus Petunia
ao Renato Stehmann, Aline P. Lorenz-Lemke, Loreta B. Freitas,
Abstract The common garden petunia, Petunia hybrida, is derived from P. integri-
folia and P. axillaris,twoofmanyPetunia species endemic to South America. The
geographic distribution includes temperate and subtropical regions of Argentina,
Uruguay, Paraguay, Bolivia, and Brazil, with a center of diversity in southern Brazil.
The presence of seven chromosomes and a number of morphological, anatomical,
and biochemical characteristics differentiate the genus from its sister taxon, Calibra-
choa. Included in this chapter is a taxononomic guide for the 14 currently recognized
species, some of them restricted to very small geographic areas. Species diversity is
in danger of diminishing signiﬁcantly due to human intervention, particularly in the
form of grassland destruction.
1.1 Historical Review
Petunia Jussieu (Solanaceae) is best known for the garden petunia, an ornamental
hybrid widely cultivated around the world. There are many cultivars with a broad
range of ﬂower color and size, and the market of their seeds represents an impor-
tant economic resource for many countries. Its generic epithet comes from “petum”
or “betum,” an indigenous name given to the tobacco, Nicotiana tabacum L., that
roughly resembles one of the ﬁrst two species described in Pet u n i a , P. nyctaginiﬂo r a
Juss. (=P. axillaris [Lam.] Britt. et al.) (Fries 1991). Due to some morphological
similarities, such as annual growth habit, ﬁve stamens, capsular fruits, and small
seeds, Petunia and Nicotiana G. Don were historically included in the same infra-
familiar taxonomic groups (Wettstein 1895; D!Arcy 1991; Hunziker 1979, 2001).
However, recent phylogenetic studies based on molecular data suggest that Nico-
tiana and Petunia are not so closely related and should be placed in different subfam-
ilies (Olmstead and Palmer 1992; Olmstead, Sweere, Spangler, Bohs, and Palmer
1999; Olmstead and Bohs 2007).
J.R. Stehmann (B)
Departamento de Botˆ
anica, Instituto de Ciˆ
ogicas, Universidade Federal de Minas
Gerais, Av. Antˆ
onio Carlos 6627, 31270-110, Belo Horizonte, MG, Brazil
T. Gerats, J. Strommer (eds.), Petunia,DOI10.1007/978-0-387-84796-2 1,
"Springer Science+Business Media, LLC 2009
2 J.R. Stehmann et al.
Petunia was originally described by Jussieu (1803) based on material collected
in Montevideo, Uruguay, by Commerson. Two very distinct species, P. parviﬂora
and P. nyctaginiﬂora, were described in the same paper, the ﬁrst with short fun-
nelform corolla and the second salverform with a long corolla tube. Earlier, in 1793,
Lamarck described the latter species as Nicotiana axillaris Lam. During the next
four decades, species of Petunia were variably described in different genera of the
Solanaceae such as Nicotiana (Lehmann 1818), Fabi a n a Ruiz & Pav. (Saint-Hilaire
1824), Calibrachoa La Llave & Lex. (La Llave and Lexarza 1825), Salpiglossis
Ruiz & Pav. (Hooker 1831), and Nierembergia Ruiz & Pav. (Graham 1833).
In 1846, Miers published a revision of the South American Solanaceae in which
he recognized 10 species of Petunia, half of them described for the ﬁrst time. His
illustrations of the species were presented later, in 1850. In the same year, but two
months later, Sendtner published his revision of Solanaceae in the Flora Brasilien-
published in 1852, Dunal presented 16 species of Petun i a , transferred another three
from Petunia to Fabiana, and described a new genus, Leptophragma, now consid-
ered a synonym of Calibrachoa.
Fries (1911) published the ﬁrst monograph of Petunia,accepting27species,nine
of which were new. The taxonomic treatment provided a detailed discussion of the
morphology, circumscription, geographic distribution, and relationships of Petunia
with other genera. Fries’ monograph remains the latest complete revision of the
genus available. During the following ﬁve decades, few new species were described
(Sandwith 1926; Steere 1931; Morton 1944). The number of species in Petunia
increased signiﬁcantly only when Smith and Downs (1964, 1966) described nine
new species among the ﬂora of Santa Catarina, Brazil.
The study of the garden petunia, termed Petunia x hybrida (Hook.) Vilm. and now
commonly known as Petunia hybrida,wasdecisiveforthefutureofthetaxonomyof
the genus. The garden petunia was ﬁrst obtained by hybridization in 1834 by Atkins
of Northampton, a British nurseryman, and it soon spread to European gardens (Sink
1984). Today it is cultivated all over the world and is one of the most important
Solanaceae utilized for ornamental purpose.
Many authors have investigated the origin of this garden hybrid and the mech-
anisms of genetic incompatibility found in Petunia (Ferguson and Ottley 1932;
Mather 1943; Mather and Edwardes 1943; Stout 1952; van der Donk 1974; Linskens
1975; Sink 1984; see Chapter 5), and different species have been suggested as par-
ents of the garden petunia.
In 1982, Wijsman considered the origin of the hybrid and concluded that it was
obtained from breeding of only two biological species, one with white ﬂowers [P.
axillaris (Lam.) Britton et al.], and the other with purple ﬂowers [P. integrifolia
(Hook.) Schinz & Thell.], each one with geographic subspecies. Later, Wijsman
(1983) tried to breed other species (P. calycina and P. linearis,2n=18)withthe
parents of the garden petunia (2n= 14). While hybrids were obtained by cross-
ing species with equivalent chromosome number, all crossings between species
with different chromosome numbers failed. Wijsman and de Jong (1985) concluded
that these groups distinguished by chromosome number (and some morphological
characters) must be treated as different genera and proposed to keep in Petunia only
the species related to Petunia parviﬂora Juss. (2n=18),thetypespeciesofthegenus
as established by Britton and Brown (1913) using the mechanical method of typiﬁ-
cation (ﬁrst species cited in the protologue). Species of Petunia with 2n=14were
transferred to Stimoryne Raﬁn., the next generic available synonym.
As the taxonomic proposal of Wijsman and de Jong (1985) would change the
name of the garden petunia, Wijnands and Bos (1986) proposed to conserve Petunia
nyctaginiﬂora Juss. (2n=14)asthetypeofPet u n i a . This proposal was accepted
(Greuter et al. 1994), and those species related to Petunia parviﬂora (2n=18)were
transferred to Calibrachoa (Wijsman 1990; Stehmann and Semir 1997; Stehmann
and Bohs 2007).
Further cytotaxonomic, reproductive, anatomical, and chemical studies related to
species of Petunia and Calibrachoa have corroborated Wijsman’s decision to split
Petunia into two genera. All species investigated in Petunia have a chromosome
number of n= 7 (Watanabe et al. 1996a), while in all Calibrachoa species examined
to date, n=9or18(Stehmann,Semir,Dutilh,andForni-Martins1996;Watanabe
et al. 1996b). Chromosome counts assign the basic numbers of x=7andx=9to
Petunia and Calibrachoa, respectively. Interspeciﬁc cross-incompatibility between
Petunia species with different chromosome numbers, as reported by Wijsman (1983)
and Watanabe et al. (1996a), demonstrates that the groups are genetically isolated
and they could not hybridize in natural conditions, even if they share the same pol-
linators. Anatomical features are useful to distinguish the genera. Reis, Sajo and
Stehmann (2002) studied leaf anatomy in 16 species of Calibrachoa and seven
species of Petunia. Fourteen Calibrachoa species have endodermis surrounding
the vascular bundles, formed by well-developed parenchymatic cells very distinct
from surrounding mesophyll. Only two species, C. parviﬂora (Juss.) D!Arcy and
C. pygmaea (R.E. Fries) Wijsman, do not show differentiated endodermis. In none
of the analyzed species of Petunia is the endodermis morphologically differenti-
ated. Chemical evidence also supports Wijsman and de Jong (1985). Ellinger, Wong,
Benson, Gafﬁeld, and Waiss (1992) reported that C. parviﬂora yielded none of the
ergostanoids that are associated with Petunia species. However, only a few species
were studied and further work is needed.
Phytogenetic relationships have been clariﬁed by the results of recent molecular
studies. The separation into two genera was supported by RFLP chloroplast DNA
(Ando et al. 2005b) and ITS, cpDNA and mtDNA analyses (Kulcheski et al. 2006).
In both analyses, Petunia and Calibrachoa showed a close phylogenetic relationship
and, for this reason, are considered sister groups.
1.2 Morphological Circumscription of Petunia and Calibrachoa
Some species of Petunia and Calibrachoa have sympatric distributions and share
similar vegetative and ﬂoral attributes, making it difﬁcult to recognize the genus to
which they belong. To help with the recognition of each genus, we compare the
principal diagnostic morphological traits below (Table 1.1).
4 J.R. Stehmann et al.
Table 1.1 Comparative morphological traits between Petunia Juss. and Calibrachoa La Llave &
Trait Petu n i a Cali b rach o a
Habit Herbs with non-woody stems Small shrubs or herbs, woody
Duration Usually annual Annual or perennial
Brachyblasts Absent Present or absent
Leaves Ovate, elliptic, oblong, or obovate,
rarely linear; ﬂat margin
Ovate, elliptic, obovate, oblong, or
linear; ﬂat or revolute margin
Inﬂorescence Monochasial with opposite
Monochasial with opposite
Aestivation Imbricate Reciprocative (except in
Symmetry Actinomorphic or zygomorphic Zygomorphic (except in
Calyx Ribs usually not conspicuous;
deeply lobed (except in
P. altiplana and some coastal
populations of P. integrifolia);
lobes linear or enlarged toward
Five or ten ribs; lobed usually to
the middle, lobes usually
narrowed toward the apex
Corolla Funnelform, campanulate, or
salverform; purple, red (bright
or orange), pink, or white
ventricose, and apically
constricted in C. pygmaea);
purple, red, pink, or whitish
Anthers Yellow, bluish, or violet Yellow
Seed coat Cells with wavy anticlinal walls Cells with straight anticlinal walls
In nature, Petunia species are mostly annual with herbaceous stems and brachy-
blasts absent or poorly developed. It is difﬁcult to get information about life history
from herbarium material; additional information can be obtained by growing plants
in greenhouses, but there they do not behave as they do in nature, especially in the
subtropical regions where most species of Petunia grow. In southern Brazil the win-
ter is very cold, with minimum temperatures below 0◦C; thus, frost and snow must
affect the survival of individuals. Since Petunia species are usually not ligniﬁed and
they lack any special underground system (except for coastal populations of P. inte-
grifolia), we can assume that most species, such as P. axillaris,P. integrifolia,P.
reitzii L.B. Sm. & Downs, and P. bonjardinensis T. An do & Hashim. , a r e a n n uals.
Calibrachoa species are annual or perennial. The perennials have a shrubby habit
with basal woody stems, often bearing brachyblasts.
Leaf morphology in Petunia is more uniform than in Calibrachoa.InPetunia
the leaves are usually sessile, more rarely petiolate, ovate, obovate, or elliptic,
rarely linear, and the surface and margin are ﬂat. In Calibrachoa,leavesarealso
commonly sessile, but their form is extremely variable. There are elliptic, ovate,
obovate, oblong, and linear leaves, with ﬂat or revolute margins. The revolute mar-
gin is not found in any Petunia species. Reis et al. (2002) showed that leaves of
Calibrachoa are quite diversiﬁed, both externally and internally, and its species can
be separated according to the type of margin, distribution of stomata on leaf sur-
faces, organization of the mesophyll, and morphology of trichomes.
The inﬂorescences in both genera are sympodial, with monochasial growth,
whereby each ﬂower is always associated with two opposite, leaf-like bracts
(one sympodial unit). The sympodial pattern is typical for almost all species of
Solanaceae (Bell and Dines 1995). Secondary branches arise subsequently in the
axils of basal bracts, whereupon the appearance of the inﬂorescence may become
dichasial. Development of the sympodial unit is normally continuous, but sometimes
it can be interrupted such that the ﬂower is not produced at a speciﬁc node. Fries
(1911) and Danert (1958) described and illustrated the characteristic inﬂorescence
branching of Petunia s.l. To distinguish Petunia and Nicotiana, Smith and Downs
(1966) as well as Hunziker (1979) described Petunia with solitary ﬂowers. How-
ever, the ﬂowers of Petunia and Calibrachoa cannot be considered solitary, because
they are arranged in a sequence of sympodial units that constitute an inﬂorescence.
These sympodial units with two opposite leaf-like bracts are unique to Petunia and
Calibrachoa in Petunioideae, and clearly constitute an apomorphic character of this
The calyx of most Petunia species is deeply lobed with linear or spatulate lobes,
usually enlarged toward the apex. Calyx lobed to the middle appears only in ﬂowers
of P. altiplana T. A n d o & H ashim. and c o a s t al populat i o n s o f P. integrifolia. In
Calibrachoa the calyx is usually lobed to the middle, and the lobes are often acute
and narrowed toward the apex. Exceptions can be found in C. micrantha (R.E. Fries)
Stehmann & Semir and C. pygmaea,inwhichthecalyxcanbecleftupto2/3of
its length. However, the lobes of the calyx of C. micrantha are ovate-lanceolate
and narrowed at the apex, while in C. pygmaea they are linear and obtuse at the
apex. Another useful characteristic of the calyx is the presence of marked ribs. In
Calibrachoa, calyx ribs are prominent in most species, except in C. pygmaea and C.
Petunia species lack calyx ribs.
Fries (1911) and Smith and Downs (1966) used the degree of calyx partition as
a diagnostic characteristic in Petunia s.l. Wijsman and de Jong (1985) observed that
this distinguished most species belonging to the groups with different chromosome
numbers. The deeply lobed calyx described in P. parviﬂora [= C. parviﬂora]was
considered by them to be an artifact and treated as a pentapartite, not pentaﬁd, calyx
with lobes connected to a thin membrane. The halfway-lobed calyx of most Cal-
ibrachoa may reﬂect the higher level of fusion of the lobes and the lateral veins,
forming ten thick ribs. These ribs are quite evident in the calyx of the other related
genera, such as Fabi a n a (Barboza and Hunziker 1993) and Nierembergia (Millan
1946), in which the level of fusion is higher.
Studies on vasculature and structure of the calyx are important to the taxonomy
of Solanaceae. D’Arcy (1986) described the solanaceous general calyx as a whorl of
ﬁve lobes nerved by ﬁve primary traces that branch into the lobes, forming a pair of
lateral veins with minor leaf-like venation. He pointed out a tendency of the calyx
lobe and veins to fuse in different levels, giving rise to main traces or ribs in the
6 J.R. Stehmann et al.
fused area. In Lycianthes the calyx nervation consists of primary traces with fused
laterals leading to ten teeth in two series, and this pattern serves to distinguish it
from Solanum, with which it shares poricidal anthers.
Calibrachoa and Petunia have different aestivation patterns, and this trait distin-
guishes the genera. Petunia species show imbricate aestivation (Fig. 1.1A), whereas
most Calibrachoa species have reciprocative aestivation (Fig. 1.1B). This term was
coined by Miers for instances in which the anterior induplicative lobe covers the
four others, which are conduplicate (Hunziker 2001). Within Calibrachoa, only the
C. pygmaea corolla seems to have an imbricate-reciprocative aestivation.
Aestivation was conﬁrmed as an unambiguous characteristic that differentiates
Calibrachoa and Petunia species, as Wijsman and Jong (1985) predicted. The
Calibrachoa aestivation pattern is similar to the conduplicate pattern described
for Nicotiana by Goodspeed (1954). However, in Nicotiana the conduplicate type
is extremely variable in its degree of spirally. Within one species, N. tomentosa
Ruiz & Pav., conduplication shifts via intermediate races into imbrication. In the
Solanaceae, aestivation has long been used to distinguish subtribes (Baehni 1946)
or tribes (Hunziker 1979). The distinct ontogenetic patterns of corolla development
observed in buds of Petunia and Calibrachoa provide evidence that they are not
Fig. 1.1 Distinct patterns of corolla aestivation in Petunia and Calibrachoa.(A)Petunia exserta
with imbricate aestivation. (B)Calibrachoa sellowiana with reciprocative aestivation. Seed coat of
Petunia and Calibrachoa observed by SEM: (C) anticlinal walls are wavy in Petunia (P. integrifo-
lia)and(D) straight in Calibrachoa (C. dusenii)
closely enough related to represent infrageneric taxa, for example, subgenera, but
rather support their distinction at the generic level.
The general ontogenetic pattern of corolla aestivation is completely different
in the two genera. After initiation of the corolla primordia, the lobes start the
differentiation and growth process. The corolla lobes in Petunia become imbri-
cate at the median stage of development, before elongation of the tube. At this
same stage of bud development, corolla lobes in Calibrachoa become folded and
aestivation shows an induplicate pattern. Later the one basal lobe turns upward,
enfolding the four others. Anatomical studies are necessary to better describe these
The corolla color in Calibrachoa and Petunia species is usually purple, but both
genera may also show whitish, reddish, or pinkish ﬂowers. Species with a fun-
nelform corolla may have a yellow corolla throat in Calibrachoa,butinPetunia
yellow is never associated with this type of ﬂower. It is also worthwhile to note the
yellow color of the anthers in all Calibrachoa,butrangingfromyellowtobluishor
violet in Petunia. Ando et al. (1999) studied in detail the occurrence of ﬂoral antho-
cyanins in 20 taxa of Petunia and recognized four distinctive colors: white, purple
(and red-purple), orange-red, and bright red.
The corolla shape typically found in Calibrachoa is funnelform. Only C. pyg-
maea shows a salverform, ventricose, and apically constricted corolla. Petunia
shows various types of corolla, such as funnelform, campanulate, and salverform
(Fig. 1.2). The limb is also quite diverse in Petunia,withlobesrounded,obtuse,
retuse, or acute. In P. e x s e r t a Stehmann, a hummingbird-pollinated species, the
corolla lobes become more cleft and reﬂexed with age.
Petunia and Calibrachoa have small foveolate-reticulated seeds (less than
1.4 mm), and seed coats observed under SEM show different patterning. Seed-coat
anticlinal walls are wavy in Petunia (Fig. 1.1C) and straight in Calibrachoa (Fig.
1.1D). Bahadur, Venkateshwarlu and Swamy (1989) had previously described the
different patterns of seed-coat morphology in Petunia s.l., but did not make any
comments about the taxonomic implications of their discovery. Stehmann and Semir
(1997) reported seed-coat epidermal cells as a fundamental diagnostic characteris-
tic to distinguish the two genera. In order to check the assumption of those authors,
Watanabe et al. (1999) studie d s e e d c o a t s i n 4 5 t a x a o f t h e g e n u s Petunia s.l. Three
different seed-coat epidermal patterns were described: (1) wavy middle lamellae and
anticlinal walls, (2) wavy middle lamellae embedded in straight anticlinal walls, and
(3) straight middle lamellae and anticlinal walls. In fact, these three groups corre-
spond to the two groups, one with wavy anticlinal walls (Petunia species) and the
other with straight anticlinal walls (Calibrachoa species). The middle lamellae are
not well characterized by SEM, and the results of this analysis must be treated with
caution. The seed-coat epidermis, associated with aestivation pattern, clearly distin-
guishes Petunia from Calibrachoa.
There are few SEM descriptions of seed coats for related genera in Solanaceae.
In Nicotiana seed-coat epidermal cells, there are variable types of anticlinal walls.
Most Nicotiana species have wavy anticlinal walls, but straight anticlinal walls also
occur in this genus (Goodspeed 1954). Features of the seed-coat epidermal wall
8 J.R. Stehmann et al.
Fig. 1.2 Major patterns of Petunia ﬂower arrangements. Salverform corolla: (A)P. axillaris subsp.
axillaris; (B)P. axillaris subsp. parodii;(C)P. exserta; (D)P. mantiqueirensis;(E)P. secreta.
Funnelform or campanulate corolla: (F)P. altiplana;(G)P. bonjardinensis; (H)P. integrifolia; (I)
P. reitzii; (J)P. scheideana. Scale bar = 1 cm
are characteristics known to have taxonomic importance in Physalis (Axelius 1992)
and Schwenckia (Carvalho, Machado and Bovini 1999), as well as in other families
like Cactaceae (Barthlott and Voit 1979) and Campanulaceae (Shetler and Morin
1986). Seed-coat attributes have been considered valuable characteristics to recog-
nize species or genera, or even tribes and subtribes (Barthlott 1981).
Petunia comprises annual or perennial herbs, up to 1 m tall, with erect, ascendant,
decumbent, or procumbent stems, rarely rooting at the nodes. The leaves are sessile
or petiolate, with blades elliptic, ovate or obovate, more rarely rounded or linear,
membranaceous, somewhat juicy, ﬂat, and usually without marked venation. Inﬂo-
rescences are sympodial, with monochasial growth, whereby each ﬂower is always
associated with two opposite, leaf-like bracts. The calyx is green, deeply lobed, with
The corolla is funnelform, campanulate, or salverform, with imbricate aestivation,
tube 1.5–7 cm long, and purple, white, red (bright or orange), or pink limb. The ﬁve
stamens are variously adnated to the corolla tube, usually included and arranged in
three levels: one short, two middle, and two longer (more rarely only in two lev-
els). Anthers are ventriﬁxed, yellow or violaceous in color. The ovary is glabrous,
surrounded by a lobed nectary, with ﬁliform style, and disciform or lobed stigma.
The stigma can be placed among the anthers of the didynamous pair of stamens,
at the same level or above the longest pair, sometimes exserted to the corolla tube.
The fruits are capsular, many seeded, with peduncle inﬂexed or deﬂexed at mature
stage. Seeds range in size from 0.4 to 1.4 mm long and present seed coats with wavy
We recognize 14 speci e s d i s t r i b u t e d i n s u b t r o p i c a l a n d t e m p e r a t e S o u t h A m e r i c a .
Petunia axillaris and P. integrifolia,parentstothefamiliargardenhybrid,havethe
largest distribution. Several species are narrow endemics, for example, P. bajeensis
T. An d o & H a s h im.,P.bonjardinensis,P.exserta,P.mantiqueirensisT. A n do &
Hashim., P. reitzii, P. saxicola L.B. Sm. & Downs,and P. secreta Stehmann & Semir.
Species of Petunia can be found in sunny, partially shaded, or completely shaded
sites. Petunia altiplana, P. axillaris, P. inﬂata, and P. integrifolia are easily found in
disturbed places such as roadside slopes, especially in rocky ground; P. scheideana
and P. mantiqueirensis occur in partial shade at edges of Araucaria forests; and
P. e x s e r t a grows in the shaded relief from shallow caves sculpted by the wind in
The morphological circumscription of certain species is not easy, especially those
related to P. integrifolia, characterized by purple and funnelform corolla, violaceous
pollen, and stigma placed among the anthers of the didynamous pair of stamens.
In a wide sense, this group corresponds to Wijsman’s P. integrifolia complex (P.
integrifolia, P. inﬂata, and P. occidentalis R.E. Fr.) and others to speciﬁc (P. inte-
rior T. An d o & H a s h im., P. riograndensis T. Ando & Hashim. , P. littoralis L.B.
Sm. & Downs and P. bajeensis)andinfraspeciﬁc(P. integrifolia subsp. depauperata
(R.E.Fr.) Stehmann) taxa. This complex group of taxa called “integrifolia” com-
prises at least four distinct genetic lineages (Lorenz-Lemke, unpublished data).
A key to recognizing the species of Petunia is presented below, together with
comments about morphology, nomenclature, geographic distribution, and habitat.
1.3.1 Key to the Native Species of Petunia
1a. Corolla salverform (tube cylindrical or slightly enlarged toward the apex).
2a. Corolla white. 2. P. axillaris
2b. Corolla purple or reddish.
3a. Corolla purple; anthers and stigma included in the corolla tube; heliophilous
4a. Plant erect; corolla tube and throat purple; ﬁlaments adnate nearly to middle
of corolla tube; pollen yellow. 14. P. secreta
4b. Plant procumbent, ascendant or climbing; corolla tube and throat whitish and
purple reticulate-veined; ﬁlaments adnate below the middle of tube; pollen
bluish or violet. 9. P. m a n t i q u e i r e n s i s
10 J.R. Stehmann et al.
3b. Corolla reddish; anthers and stigma exserted from corolla tube; sciophilous
plants. 5. P. exserta
1b. Corolla funnelform or campanulate (tube clearly enlarged toward the apex).
5a. Corolla pink to bright red.
6a. Filaments adnated >9mmtocorollatubebase;stigmaslightlyexsertedabove
the anthers of longest pair of stamens. 12. P. s a x i c o l a
6b. Filaments adnated up to 8 mm to corolla tube base; stigma located below the
anthers of the longest pair of stamens. 11. P. reitzii
5b. Corolla purple.
7a. Stigma exserted above anthers of the longest stamens. 4. P. b o n j a r d i n e n s i s
7b. Stigma located at the same level or below the anthers of the longest pair of
8a. Stigma located at the same level to the anthers of the longest pair of stamens;
corolla throat pale purple to whitish with contrasting deep-purple reticulation;
stigma >1.5 mm long, vertically two lobed. 13. P. s c h e i d e a n a
8b. Stigma located below the anthers of the longest pair of stamens; corolla throat
purple with dark purple stripes or reticulation; stigma <1.2 mm long, not two
lobed (except P. occidentalis).
9a. Plant repent, rooting at the nodes; leaves widely obovate or orbicular, usually
rounded to the base, more rarely attenuate or short attenuate; calyx halfway
lobed. 1. P. a l t i p l a n a
9b. Plant erect, ascendant or decumbent, not rooting at the nodes; leaves ovate,
elliptic, oblanceolate, or obovate, rarely orbicular, with attenuate or long-
attenuate base; calyx deeply lobed (less so in coastal populations) (Petunia
10a. Anthers with channeled lobes at dehiscence. 8. P. i n t e r i o r
10b. Anthers with lobes ﬂat at dehiscence.
11a. Plant viscid; leaves with prominent venation; corolla mouth reniform in frontal
view, with intruded throat. 3. P. b a j e e n s i s
11b. Plant not obviously viscid; leaves with obscure venation; corolla mouth elliptic
in frontal view, with ﬂat throat.
12a. Stems decumbent; capsule subglobose with peduncle deﬂexed.
7. P. integrifolia
12b. Stems usually erect or ascendant; capsule ovoid with peduncle inﬂexed or
13a. Corolla limb 25–40 mm in diameter, ﬁlaments adnated <5mmtothecorolla
tube base. 6. P. i n ﬂ a t a
13b. Corolla limb 20–25 mm in diameter, ﬁlaments adnated >7mmtothecorolla
tube base. 10. P. o c c i d e n t a l i s
1. Petun ia altipla na T. Ando & H a s h i m. (Figs. 1. 2 F a n d 1 . 3A–B) – Thi s s p e c i es
is easily recognized by its rooting stems, usually broadly spatulate leaves, purple
corolla, and stigma located below the anthers of the longest pair of stamens. Its
repent habit of usually forming a round mat is unique to the genus. The radial growth
pattern plus the massive blooming permit the use of the species for ornamental
Fig. 1.3 Petunia species. (A)and(B)P. altiplana;(C)P. axillaris;(D)P. bajeensis;(E)P. bonjar-
purposes. This species is distributed in the highlands of Santa Catarina and Rio
Grande do Sul, Brazil, in altitudes from 800 to 1200 m, and grows in outcrops or
exposed roadside slopes (Ando and Hashimoto 1993).
2. Petunia axillaris (Lam.) Britton et al. (Figs. 1.2A–B and 1.3C) – It can
be readily identiﬁed by its erect habit, salverform white corolla, yellow pollen,
and inﬂexed pedicel in fruit stage. The ﬂowers emit a scent at dusk and are vis-
ited by sphingid hawkmoths (Galeto and Bernardello 1993; Ando et al. 2001;
12 J.R. Stehmann et al.
see Chapter 2). It exhibits the largest geographic distribution in the genus and
is known to occur in Brazil (Rio Grande do Sul), Argentina, Uruguay, Paraguay,
and Bolivia. Three allopatric subspecies have been accepted based on corolla tube
length and stamen arrangement (Ando 1996; Kokubun et al. 2006). Individuals of
P. axillaris are heliophilous and inhabit rocky sites, but can also be found along
3. Petun ia bajeens is T. Ando & H a s h i m . (Fig. 1.3D ) – T h e s p ecies is cha r a c -
terized by its viscid vestiture, foliose stems forming a cushion-like structure, ovate,
elliptic, or oblong leaves with prominent primary and secondary veins (showing
the marked brochidrodomous venation), purple funnelform corolla, stamens adnated
more than 7 mm to the base of the corolla tube, stigma located below the anthers
of the longest pair of stamens, and deﬂexed pedicel in fruit stage. Vegetatively, the
individuals of this species roughly resemble more robust plants of P. bonjardinensis,
but the morphology of the ﬂowers does not differ from that of P. integrifolia except
for the larger size of the ﬂoral parts. To date found only in the extreme southern
region of Rio Grande do Sul, Brazil, in the municipalities of Baj´
e, Canguc¸u, and
Lavras do Sul, it can be found growing along roadside slopes (Ando and Hashimoto
4. Petun ia bonjard inensis T. Ando & Ha s h i m . ( Figs. 1.2G a n d 1 . 3 E) – The
decumbent habit, with very fragile stems, villose vestiture, campanulate and pur-
ple corolla, stigma positioned above the anthers of the longest pair of stamens, and
deﬂexed peduncles in fruit stage are characters permitting clear identiﬁcation of the
species. Petunia bonjard i n e n s i s is endemic to a small area near to the border of the
southern Brazilian plateau, in the municipality of Bom Jardim da Serra, Santa Cata-
rina (Ando and Hashimoto 1993), where it is not difﬁcult to ﬁnd individuals growing
on roadside slopes.
5. Petunia exserta Stehmann (Figs. 1.2C and 1.3F) – Petunia exserta is unique
in the genus, showing red (red-orange) corolla and distinct exserted stamens
and stigma, attributes associated with hummingbird pollination (Stehmann 1987;
Lorenz-Lemke et al. 2006; see Chapter 2). It shares the erect habit, salverform
corolla, yellow pollen, and inﬂexed stalk with P. axillaris and P. secreta. This strictly
endemic species is known only from the “guaritas” and adjacent areas, at the munic-
ipality of Cac¸apava do Sul, Rio Grande do Sul, Brazil, growing in shallow caves
sculpted by the wind in sandstone towers.
6. Petun ia inﬂata R.E.Fr. –Pet u n i a i n ﬂ a t a can be recognized by its ascendant
habit, purple corolla with slightly constricted tube, and capsule with usually inﬂexed
fruit-stalk. This species was originally described as differing from P. violacea [=P.
graphic distribution (Fries 1911). Smith and Downs (1966) considered P. inﬂata a
synonym of P. integrifolia, but Wijsman (1982) resurrected the taxon at the sub-
speciﬁc level under P. integrifolia, awidespreadspeciesinsouthernSouthAmerica
with three geographic subspecies: P. integrifolia susbp. integrifolia,P. integrifolia
subsp. inﬂata (R.E.Fr.) Wijsman, and P. integrifolia subsp. occidentalis (R.E.Fr.)
Wijsman. In a recent study based on morphometric analysis of cultivated material,
Ando et al. (2005a) accepted P. inﬂata as distinct from P. integrifolia and pointed
out the unfolded and straight calyx lobes as useful diagnostic characters. They also
reported the existence of a hybrid zone in northwestern Rio Grande do Sul, Brazil.
7. Petunia integrifolia (Hook.) Schinz & Thell. (Figs. 1.2H and 1.4A)–This
species is recognized by the following suite of morphological characters: decumbent
stems, elliptic or obovate leaves (linear in some coastal populations), funnelform
purple corolla, anthers completely opened (ﬂat) after dehiscence, showing the bluish
pollen, stigma placed below the anthers of the longest pair of stamens, and deﬂexed
pedicels in the fruiting state. Petunia integrifolia inhabits the Pampas province and
occurs in Argentina, Uruguay, and southern Brazil (from Rio Grande do Sul to the
coast of Santa Catarina), growing on different kinds of substrata (latossols, sand-
soils, and litosoils). It can also be found on disturbed areas such as roadsides or cul-
tivated lands. This species was described and illustrated for the ﬁrst time by Hooker
in 1831 as Salpiglossis integrifolia, based on a cultivated plant at Glasgow Botanic
Fig. 1.4 Petunia species. (A)P. integrifolia;(B)P. mantiqueirensis;(C)P. scheideana;
(D)P. saxicola;(E)P. reitzii;(F)P. secreta
14 J.R. Stehmann et al.
Garden. These cultivated materials were obtained from seeds brought from Buenos
Aires by John Tweedie in the autumn of 1830. Two years later, Lindley described
and illustrated Petunia violace a , also based on plants obtained from Buenos Aires.
For a long time, this synonym was employed as the valid name of the species in
horticultural and genetic literature.
Populations growing in the sandy soils of beaches within Santa Catarina island, in
Santa Catarina State, with elongated stems bearing narrow and glabrous leaves, were
described by Smith and Downs (1966) as a different species, named P. littoralis.
Ando et al. (1995), analyzing the morphological characters of infraspeciﬁc taxa of
P. integrifolia,concludedthatP. littoralis does not differ enough to be considered
var. depauperata (R.E.Fr.) L.B.Sm. & Downs [= P. integrifolia subs. depauperata
Based on analysis of morphological and molecular data (Lorenz-Lemke unpub-
lished data), Stehmann and Bohs (2007) accept two subspecies: P. integrifolia subsp.
integrifolia and P. integrifolia subsp. depauperata (Fries) Stehmann & Semir. The
former is widespread in the Pampean region of Argentina and Uruguay, as well as in
the continental southern part of Rio Grande do Sul, Brazil, while the latter occupies
the quaternary deposits along the coast, from the extreme southern Rio Grande do
Sul to Florian´
opolis, in Santa Catarina.
Ando and Hashimoto (1998) described P. riograndensis growing in the Serra do
Sudeste, a low-altitude mountain range (600 m) that crosses southern Rio Grande
do Sul, Brazil, in an east–west direction. The main morphological character dis-
tinguishing P. integrifolia from P. riograndensis is the presence of ﬁve grooves on
the outer surface of the cylindrical portion of the corolla, observed when the calyx
is removed. In all other vegetative and ﬂoral traits, individuals of P. riograndensis
resemble those of P. integrifolia, and they could be included in the range of varia-
tion within the latter species. For this reason, P. riograndensis is here considered a
synonym of P. integrifolia.
Chen et al. (2007) analyzed the genus based on Hf1 gene sequences, and their
results corroborate that the four taxa, P. integrifolia (including the two infraspeciﬁc
taxa), P. riograndensis and P. littoralis, could be treated as conspeciﬁc. In our opin-
ion, the acceptance of a wide circumscription of P. integrifolia is the best decision
while taxonomic and evolutionary relationships are not totally clear.
8. Petun ia interio r T. Ando & G. Hash i m . –This species is extremely similar to
P. integrifolia, from which it can be distinguished only by minor characters such as
the stem often divided into three branches around the node bearing the ﬁrst ﬂower
and the channeled lobes of the dehisced anthers. After dehiscence, the anthers do
not twist as in all other species of the genus, but orient the pollen upward relative
to the ground. The ascendent stems and the corolla form and size resemble those of
P. inﬂata, but the orientation of the pedicel is different. Its geographic distribution
ranges from northwestern Rio Grande do Sul and western Santa Catarina (with some
disjunct places) in Brazil to the province of Misiones, Argentina (Ando et al. 2005a).
9. Petun ia mantiqu eirensis T. A n d o & H a shim. (Figs. 1.2D and 1.4B)–
This species is characterized by its long stems, reaching up to 4 m, petiolate,
decurrent, ovate or elliptic leaves, purple, tubulose-funnelform corolla (30–35 mm),
with reticulate-veined throat, stigma slightly exserted above the anthers at the same
level of the corolla limb, and weakly deﬂexed pedicel in fruiting stage. The geo-
graphic distribution of P. mantiqueirensis is restricted to the Serra da Mantiqueira,
in Minas Gerais, southeastern Brazil, where few populations are known. Individuals
of P. mantiqueirensis are shade tolerant and grow on the border of the Araucaria or
montane forests, as well as on more open places, at altitudes ranging from 1000 to
1700 m above sea level (Ando and Hashimoto 1994).
10. Petun ia occiden talis R.E.Fr.–Theerectorascendanthabit,thesmallﬂow-
ers with purple funnelform corolla showing a long cylindrical base (>8mm),the
weakly didynamous stamens, stigma bilobed, positioned slightly above the anthers
of the longest pair of stamens, and inﬂexed fruit-stalk are characters that clearly
distinguish this species from other Petunia. Its geographic distribution is restricted
to the Sub-Andean mountains (from 650 to 2000 m of altitude) in northwestern
Argentina (Jujuy, Salta) and southern Bolivia (Tarija), being separated from the
other Petunia species by the Chaco, a large, ﬂat region covered by a dry forest,
in northern Argentina, Bolivia, and Paraguay (Fries 1911; Tsukamoto et al. 1998).
11. Petunia reitzii L.B.Sm. & Downs (Figs. 1.2I and 1.4E) – This species is
distinguishable by its ascendent habit, bright red, funnelform corolla, with ﬁlaments
adnated less than 8 mm to the base of the corolla tube. Petunia reitzii is endemic to
the oriental border of the southern Brazilian plateau in Santa Catarina and seems to
be restricted to a small area between the municipalities of Bom Retiro and Urubici,
at altitudes of about 1000 m and associated with Araucaria forest. It grows on the
walls of small cliffs beside rivers, hanging freely in space (Ando et al. 1999), but
can also be found along exposed roadside slopes.
12. Petun ia saxicol a L.B. Sm. & Downs (Fig. 1.4D) – This species is similar to
P. r e i t z i i ,especiallyinthebrightredcolorofthecorolla,butP. saxicola has a longer
corolla tube, reaching 40–45 mm, with ﬁlaments adnated more than 9 mm to the
base of the corolla tube, stigma slightly exserted above the anthers of longest pair
of stamens, and glabrous leaves. The saxicolous habit of this species is unique in
the genus, and individuals are found growing on humid and rocky escarpments of
Otacilio Costa, Santa Catarina. Only one population of P. saxicola is known to exist.
13. Petun ia sche ideana L.B. Sm. & Downs (Figs. 1.2 J and 1.4C) – Petunia
scheideana is characterized by its very variable habit, with long-branched stems,
sometimes up to 3 m long (either procumbent, ascendant or climbing), usually
petiolate and glabrous leaves (except margin and ribs), ovate or elliptic blades,
funnelform purple corolla with short tube (13–15 mm long) showing a deep pur-
ple reticulate-veined throat, anthers of the long stamens evidently separate from
each other, pollen bluish, stigma bilobed placed at the same level as the anthers
of the longer pair of stamens, and pedicels usually elongated, weakly deﬂexed in
the fruiting stage. The geographic distribution ranges from higher altitudes (800–
1000 m) in Paran´
a and Santa Catarina, Brazil, often associated with Araucaria
forests, westward into the lowlands of extreme northern Misiones, Argentina (about
200–300 m). In Brazil, it can be found in the ecotonal zone between grasslands
16 J.R. Stehmann et al.
and forests, climbing in the shrubby or arboreal vegetation along the border of the
Araucaria forest or more spreading in open areas or roadside slopes. Nevertheless,
in Argentina, Ando, Soto, and Suarez (2005c) reported its occurrence at open road-
sides within thick forest (subtropical semideciduous forest), and not in Araucaria
Petunia guara p u a v e n s i s T. A n d o & H a shim. is tre a t e d h ere as a synon y m o f P.
scheideana. Ando and Hashimoto (1995) compared their new species only to P.
integrifolia, but not to P. scheideana, with which it shares all vegetative and ﬂoral
attributes. The geographic distribution of P. guarapuavensis is in the more conti-
nental region of the Serra Geral, the Guarapuava High Plateau and adjacent areas of
Santa Catarina, and must represent only disjunct populations of P. scheideana.
14. Petun ia secreta Stehmann & Semir (Figs. 1.2E and 1.4F) – Pe t u n i a s e c reta
is an annual, erect or ascendant, easily recognizable by its purple and salverform
corolla, yellow pollen, and erect fruit-stalk. The corolla form is shared only with P.
exserta (red-orange) and P. axillaris (white). Pet u n i a s e c r e t a is endemic to the place
called “Pedra do Segredo” and adjacent areas around the municipality of Cac¸apava
do Sul, in Rio Grande do Sul, southern Brazil. It is clearly heliophilous, inhabiting
the top of conglomerate sandstone towers at about 300–400 m elevation and visited
by bees (Stehmann and Semir 2005).
Hunziker (2001) accepted P. patagonica as belonging to the genus, but we are
considering it a doubtful name. This species was originally described under Nierem-
bergia by Spegazzini (1897) based upon material collected in San Jorge Gulf,
Argentina. Millan (1946) transferred this species to Pet u n i a , but its morphological
characters (linear leaves, solitary ﬂowers, and campanulate calyx with obtuse and
short lobes) do not match those described for the genus (Table 1.1). Further studies
are necessary to clarify the identity of this taxon
1.4 Patterns of Geographic Distribution
The genus Petunia is endemic to South America, with subtropical distribution rang-
ing from 22◦to 39◦S (Fig. 1.5). The major species richness is found in Brazil (13),
followed by Argentina (5), Uruguay, Paraguay, and Bolivia (2). All species occur in
Brazil, except for P. occidentalis, which has a disjunct distribution restricted to the
Sub-Andean mountains in northwestern Argentina and southern Bolivia.
We can distinguis h t w o p r i n c i p a l a r e a s o f o c c u r r e n c e ( c e n t e r s o f d iversity) of
Petunia species, both located in southern Brazil, where the genus must have radiated
and spread in recent times (Kulcheski et al. 2006): (a) lowlands of the Pampean
region (Fig. 1.5A) and (b) highlands of the southern Brazilian plateau (Fig. 1.5B).
The two areas, where nine species (64%) are known to occur, are included in the
Pampean and Paranense provinces, respectively (Cabrera and Willink 1980).
The area of highest richness is located at low altitudes, in a region known as Serra
do Sudeste, included in the Brazilian pampa. The Pampas occupy a vast region
in Argentina (Buenos Aires, La Pampa, Santa Fe, and C´
ordoba), Uruguay, and
Fig. 1.5 Geographic distribution of Petunia (solid lines). The two centers of diversity (dotted line)
Catarina, Brazil, are indicated, as well as the major disjunct regions (C)SerradaMantiqueira,in
Minas Gerais, Brazil, and (D)theSub-AndeanregioninArgentinaandBolivia
southernmost Brazil and are covered by temperate grasslands. The Serra do Sudeste
and neighboring places in southern Rio Grande do Sul have a low-altitude mountain
range (reaching 600 m in some areas of the Escudo Sul-Rio-Grandense) and a set
of diverse edaphic conditions. Petunia integrifolia and P. axillaris, parental species
of garden petunia, are sympatric in these areas (Ando et al. 2001). Five species of
Petunia grow in Serra do Sudeste, three of them strict endemics (P. bajeensis, P.
exserta, and P. secreta).
The second area comprises the border of the Serra Geral (a large escarpment
ranging from Minas Gerais to Rio Grande do Sul) in the state of Santa Catarina. In
this area, species of Petunia grow associated with grasslands, along forest borders,
or on outcrops associated with Araucaria moist forests, at altitudes ranging from
800 to 1800 m. For this area we can list the occurrence of four species, three of
them strict endemics, P. bonjardinensis, P. reitzii and P. saxicola, restricted to the
higher area of the plateau in Santa Catarina.
18 J.R. Stehmann et al.
There are two major disjunct areas of occurrence of Petunia:theSerradaMan-
tiqueira in Minas Gerais, Brazil, and the Sub-Andean region in Argentina and
Bolivia (Fig. 1.5C, 1.5D). In the ﬁrst, only P. mantiqueirensis is found, an endemic
species phylogenetically related to the Brazilian highland group. The geographic
barrier corresponds to the Atlantic rainforest and savanna that cover almost all the
ao Paulo state. The Sub-Andean region is separated from the core Petunia distri-
bution by the Chaco, a large and drier region, and inhabited by two taxa: P. axillaris
subsp. subandina, which grows from San Luis, Argentina, toward Tarija, Bolivia
(Ando 1996; Kokubun et al. 2006), and P. occidentalis, with distribution restricted
to northern Argentina and adjacent areas in Bolivia (Fries 1911; Tsukamoto et al.
The subtropical range of Petunia, with centers of diversity in southern Brazil,
overlaps with that of Calibrachoa. The two groups are widely separated geographi-
cally from the core distribution of the other herbaceous Petunieae (sensu Olmstead
and Bohs 2007) (except in part for Bouchetia Dunal and Nierembergia). As Petu-
nia and Calibrachoa are closely related (Kulcheski et al. 2006) and reproductively
isolated (Wijsman 1983; Watanabe et al. 1996a), we suppose that they had a con-
gruent biogeographic history with radiation and expansion. The morphological ﬂo-
ral similarity of many species of Petunia and Calibrachoa, basis of the taxonomic
generic confusion, must represent an example of convergence. Studies realized by
Wittmann, Radtke, Cure, and Schiﬁno-Wittmann (1990) indicated that some species
of both genera are melittophilous and share similar groups of pollinators. During
ﬁeld work we could observe the occurrence of syntopic pairs of mellitophilous
species of Petunia and Calibrachoa in almost all areas of southern Brazil. In Petu-
nieae, pollination by bees was reported for the genera Nierembergia (Cocucci 1991)
and Petunia s.l. (Wittmann et al. 1990). Nevertheless, species of Nierembergia are
pollinated primarily by oil-collecting bees, while Petunia and Calibrachoa are vis-
ited by bees searching for pollen and nectar (Wittmann et al. 1990; Ando et al. 2001;
Stehmann and Semir 2001).
1.5 Evolutionary Relationships and Endemic Species
Classiﬁcation of subfamilies and tribes of Solanaceae has changed signiﬁcantly in
the last decade. Using the circumscription of Fries (1911), Hunziker (1979) consid-
ered Petunia s.l. related to Nicotiana, belonging to the tribe Nicotianeae, subfamily
Cestroideae (Hunziker 1979). After the proposal of Wijsman and de Jong (1985)
and its nomenclatural consequence (Brummitt 1989), D’Arcy (1991) accepted the
genus Calibrachoa as distinct within Nicotianeae. Olmstead and Palmer (1992)
investigated subfamilial relationships and character evolution in Solanaceae based
on chloroplast DNA phylogeny, reporting that Petunia s.s. (P. axillaris with 2n=
14) and Fab i a n a constitute a sister group and that both genera plus Brunfelsia L.
might best be combined to form a new tribe. Fab i ana is a Patagonian and Andean
genus with about 15 species, consisting of small ericoid shrubs or chamaephytes
(Barboza and Hunziker 1993). It shares morphological characters with some Cal-
ibrachoa (but not Petunia), such as the woody habit, brachyblasts, linear leaves, a
funnelform corolla, and a basic chromosome number of n=9.However,theydiffer
in their geographic distributions, with Fab i a n a in the Andes, and Calibrachoa (as
well as Petunia)inthePampasandthesouthernBrazilianPlateau.
Data of Olmstead et al. (1999) based on chloroplast DNA variation delim-
ited a traditional Cestroideae as ﬁve smaller, monophyletic informal groups: Ces-
troideae, Petunioideae, Schizanthoideae, Nicotianoideae, and Schwenckioideae. But
in a recent summary published by Olmstead & Bohs (2007), the ﬁve major clades
were treated as tribes of Cestroideae, with Petunia plus eight genera placed in Petu-
nieae. The phylogenetic relationships within Petunieae remain unresolved and fur-
ther work is needed, especially in Brunfelsia, Fabiana, Leptoglossis Benth., and
The evolutionary history of Petunia Juss. has been recently investigated through
different genetic markers. Short genetic distances among the species and consequent
poorly resolved phylogenies were the general pattern, indicating recent diversiﬁca-
tion. Ando et al. (2005b) analyzed 52 taxa of Petunia s.l. by plastidial RFLP mark-
ers; Kulcheski et al. (2006) investigated 11 Petunia s.s. taxa with eight sequence
markers for the three plant genomes, and Chen et al. (2007) studied 19 Petunia s.s.
for two sequence markers, one nuclear, the other plastidial. Ando et al. (2005b)
and Kulcheski et al. (2006) detected two major groups: one corresponds to high-
land species (altitude over 800 m) and the other to lowland species (altitude below
800 m). The three papers conﬁrmed the genus monophyly, the Calibrachoa posi-
tion as the sister taxon, and the large genetic distance between the clade containing
Petunia plus Calibrachoa and the other genera of the tribe Nicotianeae.
While species description and delimitation have traditionally been based on mor-
phology, biologists have recognized that morphological divergence may have little
relationship to the degree of genetic differentiation between speciﬁc lineages (Orr
2001). Therefore, it could be difﬁcult to predict the genetic cohesiveness of a group
based on its morphological differentiation or taxonomic status alone. For instance,
Schaal, Hayworth, Olsen, Rauscher, and Smith (1998) showed many examples of
infraspeciﬁc differentiation in plants, with the occurrence of isolated lineages across
its range. On the other hand, genetic exchange between well-established, morpho-
logically distinct species is a widespread phenomenon in plants (Mallet 2005). Addi-
tionally, groups that undergo adaptive radiation frequently exhibit rapid morpholog-
ical differentiation and may present little genetic divergence and weak reproductive
barriers between species (Seehausen 2004; Ando et al. 2005b).
In recent years, a recurring claim with regard to the species problem is that
most species concepts have implicit similarities and are consistent with the idea
that species are evolving lineages or populations (Hey 2001). The phylogeographic
approach may be the needed bridge between the species concepts and empirical
studies, offering a means to understand the historical processes that have inﬂuenced
the structure of genetic variation now observed in the species (Avise 2000). Plant
phylogeographic studies, however, remain rare in comparison to those of animals,
20 J.R. Stehmann et al.
owing in part to the difﬁculty of obtaining markers with an appropriate level of
intraspeciﬁc polymorphism (Schaal et al. 1998; Shaw et al. 2005). These investi-
gations, however, increased in recent years once nuclear (Strand, Leebens-Mack,
and Milligan 1997; Olsen and Schaal 1999; Gaskin and Schaal 2002) and plastid
(Maskas and Cruzan 2000; Lorenz-Lemke et al. 2006) sequences, as well as nuclear
microsatellites (Collevatti, Grattapaglia, and Hay (2001), which exhibit adequate
variation, began to be identiﬁed. The phylogeographic approach has allowed, in
some cases, detailed understanding of populational and historical processes, espe-
cially in plants of economic and ecological interest (Schaal et al. 2003). Since phy-
logeography is applicable to problems both below and above species boundaries, its
analysis can cover a wide range of plant evolutionary patterns (Schaal et al. 1998).
Lorenz-Lemke et al. (2006) investigated the molecular diversity of the endemic
Petunia exserta and its closely related species P. axillaris subsp.parodiiand the
ﬁrst case of natural interspeciﬁc hybridization between Petunia species. P. e x s e r t a
is the only ornithophilous species of the genus and is characterized by showy red
ﬂowers with anthers and stigma strongly exserted. In spite of its exuberant color,
P. e x s e r t a is not the parent of red-ﬂower commercial hybrids, having been discov-
ered some decades after these hybrids had been produced (Griesbach, Stehmann and
Meyer 1999; Ando et al. 2000). Endemic in a very small area (about 500 km2)of
the Serra do Sudeste region, it has so far been found growing within shallow caves
in the rock (shelters) on sandstone towers, which seems to be a very restricted and
inhospitable environment for the other species of this genus (Stehmann 1987). P.
exserta and P. axillaris are closely related species (Ando et al. 2005b; Kulcheski
et al. 2006) that share diverse morphological characteristics. P. axillaris displays
white ﬂowers that emit a strong fragrance at nightfall and produce a considerable
amount of nectar to attract nocturnally active hawkmoths (Sphingidae) (Ando et al.
2001), see Chapter 2. Its distribution range includes Bolivia, Argentina, Uruguay,
and Brazil’s extreme south, and it can be found in rocky outcrops and also in dis-
turbed habitats such as the margins of highways (Ando 1996). In various locations
the distribution of P. axillaris overlaps that of the other species of the genus, and it is
possible to achieve artiﬁcial crossings between them and P. axillaris (Watanabe et al.
1996a). The analysis of trnH-psbA,trnS-trnG, and psbB-psbH chloroplast (cp) DNA
markers by Lorenz-Lemke et al. (2006) revealed 13 haplotypes, and the network
showed two main genetic clades, which probably represent the original gene pool
of the two species in the region. In general, individuals of a given population pre-
sented the same haplotype, independent of phenotype, corroborating the hybridiza-
tion hypothesis. Field observations suggest that hummingbirds are responsible for
the interspeciﬁc gene ﬂow. Analysis of molecular variance (AMOVA) revealed high
interpopulational diversity among the towers. The low rate of gene ﬂow between
populations is possibly related to the autochoric seed dispersion system, wherein
dispersion is entirely by free fall or explosive propulsion by a fruit that opens sud-
denly or by a trip lever (van der Pijl 1982).
Hybridization with a widespread congener can create serious consequences for
rare plant species (Levin, Francisco-Ortega, and Jansen 1996). The low levels of
interspeciﬁc genetic variability disclosed by diverse molecular markers (Kulcheski
et al. 2006; Lorenz-Lemke et al. 2006) indicate that the separation between P. axil-
laris and P. e x s e r t a is extremely recent. Habitat shift and modiﬁcations of ﬂoral traits
are some of the probable factors involved in the isolation between these species.
Therefore, hybridization with P. axillaris can constitute a risk for the maintenance
of P. e x s e r t a ’s typical populations, as it allows for the dilution or loss of the unique
adaptations of this species. A question that remains is whether the hybridization
between P. axillaris and P. e x s e r t a is recent (possibly related to anthropogenic dis-
turbance) or a more ancient historical process. A considerable change in the ﬂoral
composition of the Serra do Sudeste region took place with the start of more inten-
sive human colonization around 1800, as the introduction of agricultural food and
forage crops led to the almost complete degradation of the original vegetation. Some
30 endemic plant species with very restricted distributions are found in this region,
and among these, P. e x s e r t a seems to require special attention due to the factors pre-
sented here, such as very strict distribution and habitat requirements (Guadagnin,
Larocca, and Sobral 2000). Reduction in the number of individuals, and even local
population extinctions, have been documented for P. e x s e r t a (Guadagnin et al.
2000), and the species has now been added to the local list of endangered species
(http://www.sema.rs.gov.br/sema/html/pdf/especiesameacadas.pdf). In addition to
P. e x s e r t a ,theoccurrenceofotherendangeredspeciesindicatestheneedforthe
establishment of conservation units in certain Serra do Sudeste areas, especially in
the rocky outcrops where these taxa are predominantly found.
In the southern and southeastern Brazilian highlands, another Petunia group
shows morphological and genetic patterns that indicate recent speciation. Lorenz-
Lemke (unpublished data) have analyzed the sequences of plastidial markers of
seven closely related taxa (P. altiplana,P. bonjardinensis,P. guarapuavensis [treated
as a distinct species], P. mantiqueirensis,P. reitzii, P. saxicola, and P. scheideana)
that occur associated with grasslands, and link their reproductive isolation to geo-
graphic discontinuity. These species are melittophilous (pollination carried out by
bees), self-incompatible (Tsukamoto et al. 1998), and genetically close (a mono-
phyletic group, according to Kulcheski et al. 2006). As the natural pollinators are
shared and artiﬁcial interspeciﬁc crossings result in fertile hybrids (Watanabe et al.
1996a), it was suggested that geographic isolation is the major factor involved in
the maintenance of species integrity. All data suggest that the diversiﬁcation of
this “highland clade” may be a product of allopatric speciation triggered by habi-
tat range shifts through the Pleistocene period. The dating analyses by Lorenz-
Lemke (unpublished data) indicated a Pleistocene radiation and a high diversiﬁ-
cation rate, comparable to plant groups that undergo continental or island radiation
(Baldwin and Sanderson 1998; Klak, Reeves, and Hederson 2004; Hughes and East-
wood 2006). The lack of well-differentiated clades between the species and haplo-
type sharing suggest the persistence of ancestral polymorphisms through speciation
events and/or past interspeciﬁc hybridization. AMOVA revealed a high level of pop-
ulation structuring, distinct seed dispersion abilities between the species, and the
inﬂuence of the Pelotas river on the genetic structure of P. altiplana and P. b o n j a r d i -
habitat loss due to Pinus forestation and diverse agricultural use of grassland areas.
22 J.R. Stehmann et al.
The remaining grassland areas of the southern and southeastern Brazilian high-
lands are sparse and small, due to historical and current processes. Paleoenviron-
mental reconstructions from pollen records conﬁrmed that these grasslands were
natural formations that covered the Brazilian highlands uninterruptedly since at least
the last glacial age (Behling 2002). These data also demonstrated that their biodi-
versity has suffered anthropogenic disturbances since the early Holocene, with the
increase of ﬁre events probably related to the onset of occupation by Amerindi-
ans. Currently, large grassland areas have been replaced by exotic pine forests and
different agricultural practices, which represent the main threats for these ﬂoristic
formations (Behling and Pillar 2007).
The Petunia species are directly affected by grassland destruction. Besides being
restricted to this biome, the greater number have an exceptionally small geographic
distribution, the extreme situation occurring with P. saxicola,forwhichonlyone
population is known. It is not known if these micro-endemisms are natural or have
suffered anthropogenic inﬂuence. Moreover, the cpDNA results indicated that seed
ﬂow between the populations is naturally low at this biome. Furthermore, the present
changes are happening at a fast pace and can have signiﬁcant effects in the demo-
graphic dynamics of these species, especially in reducing the genetic diversity (that
already is very limited) and increasing random genetic drift effects (Ellstrand and
Elam 1993). As the largest portion of their genetic diversity is interpopulational,
most of these Petunia populations should be considered as separate management
P. r e i t z i i and P. saxicola were already included in the “List of Threatened Brazil-
ian Flora,” classiﬁed as critically endangered (2004 IUCN Red List of Threatened
genetic data obtained by Lorenz-Lemke (unpublished) suggest that P. mantiqueiren-
sis,P. bonjardinensis, and P. scheideana should also be included. Beyond their great
biological value as an endemism center, the Brazilian highlands deserve special
attention due to their remarkable ﬂora richness, shaped by the convergence of trop-
ical and temperate taxa (Rambo 1951a, b). These transitional regions are extremely
important for the diversiﬁcation and speciation processes, and to preserve popula-
tions that occur along these areas can be a protection strategy for possible biological
responses to environmental or climatic changes (Smith, Kark, Schneider, and Wayne
In the Petunia genus, the integrifolia group presents the most complex taxonomy
and comprises species, varieties, and subspecies. These taxa, in which the garden
petunia parentals are included (Petunia xhybrida pink ﬂowers), show one of the
widest distributions in South America, since they can be found in Argentina, south-
ern Brazil, and Uruguay. This set of organisms (P. integrifolia subsp. integrifolia,
P. integrifolia subsp. depauperata,P. littoralis,P. interior,P. inﬂata,P. riogranden-
sis, and P. bajeensis)presentsverysimilarmorphologicalcharacteristics,inwhich
it is difﬁcult to outline stable entities. Some ﬂoral characteristics are shared by all
these taxa, such as a magenta or purple infundibuliform corolla, violaceous pollen,
and stigma located between the anthers of the larger or median-sized stamens. On
the other hand, the considerable variation seen in vegetative character and habitat
among taxa in the integrifolia group, observed across its wide distribution area, led
to various changes in its taxonomic status through the years (Fries 1911; Smith and
Downs 1966; Wijsman 1982; Ando et al. 1995, 2005a). Species distinction is usu-
ally made by geographic distribution, as well as by overlapping vegetative and ﬂoral
Using a phylogeographic approach, Lorenz-Lemke (unpublished data) analyzed
the taxa that comprise the integrifolia group with the intent to better understand
the diversiﬁcation processes and to contribute to a more adequate delimitation of
its units. Plastidial markers showed that this group comprises four distinct lineages
clearly delimited geographically and that the actual integrifolia taxonomy should be
revised. P. bajeensis and P. inﬂata seem to form two taxonomic units independent of
the other forms of the group. Genetic differences were not found between P. integri-
folia subsp. integrifolia and P. riograndensis,betweenP. integrifolia subsp. depau-
perata and P. littoralis,orbetweenP. inﬂata and P. interior. These features sug-
gest that the few morphological characters that distinguish them are not appropriate
for taxonomic delimitation. Environmental heterogeneity (especially luminosity and
edaphic factors) and phenotypic plasticity are probably related to the morphological
variability found among its natural populations. The existence of well-established
clades indicates that these taxa are historically isolated. While the other three clades
occur in a geologically ancient area, the P. integrifolia subsp. depauperata/P. l i t -
toralis clade occurs in areas that were under strong inﬂuence of the Pleistocene
marine transgression/regressions. This lineage has its occurrence limited to quater-
nary sediments of the coastal plain of southern Brazil. Using the accurate geological
age of this area as a calibration point for the continental/coastal lineages divergence
(400,000 ybp; Villwock and Tomazelli 1995), a substitution rate was calculated.
This result will make possible better inferences about the evolutionary history of
the Petunia and its sister group Calibrachoa,situatingthediversiﬁcationeventsin
the climatic, ﬂoristic, and geologic contexts in which they occurred.
Acknowledgements We thank Conselho Nacional de Desenvolvimento Cient´
ıﬁco e Tecnol´
(CNPq) for grants to the ﬁrst three authors. We are also grateful to Marcos Sobral and Julie
Dutilh for their kind suggestions and corrections to an earlier version of our chapter and to M´
Werneck who very kindly helped us mapping Petunia distribution.
Ando, T. and Hashimoto, G. (1993) Two new species of Pe tuni a (Solanaceae) from southern Brazil.
J. Linnean Soc. Bot. 111, 265–280.
Ando, T. and Hashimoto, G. (1994) A new Brazilian species of Petunia (Solanaceae) from the
Serra da Mantiqueira. Brittonia 46, 340–443.
Ando, T. and Hashimoto, G. (1995) Petu n i a g uar a p uave n s is (Solanaceae): A new species from
planalto of Paran´
Ando, T., Kurata, M., Sasaki, S., Ueda, Y., Hashimoto, G. and Marchesi, E. (1995) Comparative
morphological studies on infraspeciﬁc taxa of Petunia integrifolia (Hook.) Schinz et Thell.
(Solanaceae). J. Jap. Bot. 70, 205–217.
Ando, T. (1996) Distribution of Petunia axillaris (Solanaceae) and its new subspecies in Argentina
and Bolivia. Acta Phytotax. Geobot. 47, 19–30.
24 J.R. Stehmann et al.
Ando, T. and Hashimoto, G. (1996) A new Brazilian species of Petunia (Solanaceae) from interior
of Santa Catarina and Rio Grande do Sul. Brittonia 48, 217–223.
Ando, T. and Hashimoto, G. (1998) Two new species of Petunia (Solanaceae) from Southern Rio
Grande do Sul, Brazil. Brittonia 50, 483–492.
Ando, T., Saito, N., Tatsuzawa, F., Kakefuda, T., Yamakage, K., Ohtani, E., Koshi-ishi, M., Mat-
susake, Y., Kokubun, H., Watanabe, H., Tsukamoto, T., Ueda, Y., Hashimoto, G., Marchesi,
E., Asakura, K., Hara, R. and Seki, H. (1999) Floral anthocyanins in wild taxa of Petunia.
Biochem. System. and Ecol. 27, 623–650.
Ando, T., Tatsuzawa, F., Saito, N., Takahashi, M., Tsunashima, Y., Numajiri, H., Watanabe, H.,
Kokubun, H., Hara , R., Seki, H. a nd Ha shimoto, G . (2000) Differenc es in the ﬂoral ant hocyanin
content of red petunias and Petunia exserta.Phytochem.54,495–501.
Ando, T., Nomura, M., Tsukahara, J., Watanabe, H., Kokubun, H., Tsukamoto, T., Hashimoto, G.,
Marchesi, E. and Kitching, I.J. (2001) Reproductive isolation in a native population of Petunia
sensu Jussieu (Solanaceae). Ann. Bot. 88, 403–413.
Ando, T., Ishikawa, N., Watanabe, H., Kokubun, H., Yanagisawa, Y., Hashimoto, G., March-
esi, E. and Su´
arez, E. (2005a) A morphological study of the Petunia integrifolia complex
(Solanaceae). Ann. Bot. 96, 887–900.
Ando, T., Kokubun, H., Watanabe, H., Tanaka, N., Yukawa, T., Hashimoto, G., Marchesi,
arez, E. and Basualdo, I.L. (2005b) Phylogenetic analysis of Petunia sensu Jussieu
(Solanaceae) using chloroplast DNA RFLP. Ann. Bot. 96, 289–297.
Ando, T., Soto, S. and Suarez, E. (2005c) New records of Petun i a (Solanaceae) for the Argentinian
ﬂora. Darwiniana 43, 1–4.
Avise, J.C. (2000) Phylogeography:The History and Formation of Species. Harvard University
Axelius, B. (1992) Testa patterns in some species of Physalis L. and some other genera in the tribe
Solaneae (Solanaceae). Intern. J. Plant Sci. 153, 448–502.
Baehni, C. (1946) L!Ouverture du bouton chez les ﬂeurs de Solan´
ees. Candollea 10, 399–492.
Bahadur, B., Venkateshwarlu, K. and Swamy, N.R. (1989) SEM Studies of seeds in nine species
of Petunia Juss. (Solanaceae). Phytomorph. 39, 121–128.
Baldwin, B.G. and Sanderson, M.J. (1998) Age and rate of diversiﬁcation of the Hawaiian silver-
sword alliance (Compositae). Proc. Natl. Acad. Sci., USA 95, 9402–9406.
Barboza, G.E. and Hunziker, A.T. (1993) Estudios en Solanaceae XXXIV. Revisi´
de Fab i ana.Kurtziana22,109–153.
Barthlott, W. and Voit, G. (1979) Mikromorphologie der samenschalen und taxonomie der Cac-
taceae: Ein raster-elektronen-mikroskopischer ¨
uberblick. Plant System. Evo. 132, 205–229.
Barthlott, W. (1981) Epidermal and seed surface characters of plants: Systematic applicability and
some evolutionary aspects. Nord. J. Bot. 1, 345–355.
Behling, H. (2002) South and southeast Brazilian grasslands during late quaternary times: A sythe-
sis. Palaeogeo. Palaeoclim. Palaeoecol. 177, 19–27.
Behling, H. and Pillar, V.P. (2007) Late quaternary vegetation, biodiversity and ﬁre dynamics on the
southern Brazilian highland and their implication for conservation and management of modern
Araucaria forest and grassland ecosystems. Phil. Trans. Royal Soc. B, 362, 243–251.
Bell, A.D. and Dines, T.D. (1995) Branching patterns in the Solanaceae. In: P.C. Hoch and A.G.
Stephenson (Eds.), Experimental and Molecular Approaches to Plant Biosystematics.Missouri
Botanical Garden, St. Louis, pp. 157–171.
Britton, N.L. and Brown, A. (1913) An Illustrated Flora of the Northern U.S. and Canada, Vol. 3.
Dover Publications Inc., NY.
Brummitt, R.K. (1989) Report of the committee for Spermatophyta: 36. Taxon 38, 301.
Cabrera, A.L. and Willink, A. (1980) Biogeograﬁa de America Latina,2nd Edn.SecretariaGeneral
de la OEA, Washington.
Carvalho, L.A.F., Machado, R.D. and Bovini, M.G. (1999) Seed coat micromorphology of Brazil-
ian species of Schwenckia. In: M. Nee, D.E. Symon, R.N. Lester and J.P. Jessop (Eds.),
Solanaceae IV: Advances in Biology and Utilization. Royal Botanic Garden, Kew, pp. 23–32.
Chen, S., Matsubara, K., Omori, T., Kokubun, H., Kodama, H., Watanabe, H., Hashimoto, G.,
Marchesi, E., Bullrich, L. and Ando, T. (2007) Phylogenetic analysis of the genus Petunia
(Solanaceae) based on the sequence of the Hf1 gene. J. Plant Res. 120, 385–397.
Cocucci, A.A. (1991) Pollination biology of Nierembergia (Solanaceae). Plant System. Evo. 174,
Collevatti, R.G., Grattapaglia, D. and Hay, J.D. (2001) Population genetic structure of the endan-
gered tropical tree species Caryocar brasiliense,basedonvariabilityatmicrosatelliteloci.Mol.
Ecol. 10, 349–356.
Danert, S. (1958) Die verzweigung der Solanaceen im reproduktive bereich. Abhandlungen der
Deutschen Akademie der Wissenschaften zu Berlin, Klasse f¨
ur Chemie, Geologie und Biologie
D!Arcy, W.G. (1986) The calyx in Lycianthes and some other genera. Ann. Missouri Bot. Garden
D!Arcy, W.G. (1991) The Solanaceae since 1976, with a review of its biogeography. In: J.G.
Hawkes, R.N. Lester, M. Nee and N. Estrada (Eds.), Solanaceae III: Taxonomy, Chemistry,
Ellinger, C.A., Wong, R.Y., Benson, M., Gafﬁeld, W. and Waiss, A.C. (1992) Diterpenes of
Calibrachoa-parviﬂora. J. Nat. Prod. (Lloydia) 55, 1477–1487.
Ellstrand, N.C. and Elam, D.R. (1993) Population genetic consequences of small population size:
Implications for plant conservation. Ann. Rev. Ecol. System. 24, 217–242.
Ferguson, M.C. and Ottley, A.M. (1932) Studies in Petun i a . II. A redescription and additional
discussion of certain species of Petunia.Amer.J.Bot.19,385–407.
Fries, R.E. (1911) Die arten der gattung Petunia. Kungliga Svenska Vetenskapsaka-demiens Han-
dlingar 46, 1–72.
Galetto, L. and Bernardello, L. (1993) Nectar secretion pattern and removal effects in three species
of Solanaceae. Can. J. Bot. 71, 1394–1398.
Gaskin, J.F. and Schaal, B.A. (2002) Hybrid Tamarix widespread in USA invasion and undetected
in Asian range. Proc. Natl. Acad. Sci., USA 99, 11256–11259.
Goodspeed, T.H. (1954) The genus Nicotiana.Chron.Bot.16,1–536.
Graham, R. (1833) Nierembergia intermedia. Edinburgh New Philosophical Journal 14: 175.
Greuter, W., Barrie, F.R., Burdet, H.M., Chaloner, W.G., Demoulin, V., Hawksworth, D.L.,
Jorgensen, P.M., Nicolson, D.H., Silva, P.C. and Trehane P. (Eds.) (1994) International Code
of Botanical Nomenclature. Koeltz Scientiﬁc Books, Konigstein.
Griesbach, R.J., Stehmann, J.R. and Meyer, F. (1999) Anthocyanins in the “red” ﬂowers of Petunia
Guadagnin, D.L., Larocca, J. and Sobral, M. (2000) Flora vascular de interesse para a conservac¸˜
na bacia do arroio Jo˜
ao Dias: avaliac¸˜
apida. In: L.H. Ronchi and A.O.C.Lobato
(Eds.), Minas do Camaqu˜
a, um Estudo Multidisciplinar. Editora Unisinos, S
ao Leopoldo, pp.
Hey, J. (2001) Genes Categories and Species.OxfordUniversityPress,Oxford.
Hooker, W.J. (1831) Salpiglossis integrifolia. Entire-leaved Salpiglossis. Bot. Mag. 58: 3113.
Hughes, C. and Eastwood, R. (2006) Island radiation on a continental scale: Exceptional rates of
plant diversiﬁcation after uplift of the Andes. Proc. Natl. Acad. Sci., USA 103, 10334–10339.
Hunziker, A.T. (1979) South American Solanaceae: A Synoptic Survey. In: J.G. Hawkes, R.N.
Lester and A.D. Skelding (Eds.), The Biology and Taxonomy of the Solanaceae. Academic
Press, London, pp. 49–85.
Hunziker, A.T. (2001) The Genera of Solanaceae. ARG Gantner Verlag KG, Ruggell.
Jussieu, A.L. (1803) Sur Le Petunia, genre nouveau de la famille dˆ
es plantes solan´
ees. Ann. Mus.
Natl. Hist. Nat. 2: 214–216.
Klak, C., Reeves, G. and Hederson, T. (2004) Unmatched tempo of evolution in Southern African
semi-desert ice plants. Nature 427, 63–65.
Kokubun, H., Naka no, M., Tsuk amoto, T., Watanabe, H., H ashimoto , G., Marchesi, E .,
Bullrich, L., Basualdo, I.L., Kao, T. and Ando, T. (2006) Distribution of self-compatible and
26 J.R. Stehmann et al.
self-incompatible populations of Petunia axillaris (Solanaceae) outside Uruguay. J. Plant Res.
Kulcheski, F.R., Muschner, V.C., Lorenz-Lemke, A.P., Stehmann, J.R., Bonatto, S.L., Salzano,
F.M. and Freitas, L.B. (2006) Molecular phylogenetic analysis of Petunia Juss. (Solanaceae).
Genetica 126, 3–14.
La Llave, P. and Lexarza, J.J.M. (1825) Calibrachoa. Novorum vegetabilium Descriptiones 2: 3.
Lehmann, J.G.C. (1818) Generis Nicotianarum Historia. Hamburg. (printed for the author)
Levin, D.A., Francisco-Ortega, J. and Jansen, R.K. (1996) Hybridization and the extinction of rare
plant species. Conserv. Biol. 10, 10–16.
Linskens, H.F. (1975) Incompatibility in Pe tuni a .Proc.RoyalSoc.London,B,188,299–311.
Lorenz-Lemke, A.P., M¨
ader, G., Muschner, V.C., Stehmann, J.R., Bonatto, S.L., Salzano, F.M. and
Freitas, L.B. (2006) Diversity and natural hybridization in a highly endemic species of Petunia
(Solanaceae): A molecular and ecological analysis. Molec. Ecol. 15, 4487–4497.
Mallet, J. (2005) Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237.
Maskas, S.D. and Cruzan, M.B. (2000) Patterns of intraspeciﬁc diversiﬁcation in the Piriqueta
caroliniana complex in southeastern North America and the Bahamas. Evol. 54, 815–827.
Mather, K. (1943) Speciﬁc differences in Petun i a .I.Incompatibility.J.Genet.45,215–235.
Mather, K. and Edwardes, P.M.J. (1943) Speciﬁc differences in Petunia.III.Flowercolourand
genetic isolation. J. Genet. 45, 243–260.
Millan, R. (1946) Revisi´
on des las especies del g´
enero Nierembergia (Solanaceae). Darwiniana 5,
Morton, C.V. (1944) Taxonomic studies of tropical American plants: A list of Uruguayan Petunias,
with one new species. Contributions from the United States National Herbarium 29, 73–74.
Olmstead, R.G. and Palmer, J.D. (1992) A chloroplast DNA phylogeny of the Solanaceae: Subfa-
milial relationships and character evolution. Ann. Missouri Bot. Garden 79, 346–360.
Olmstead, R.G., Sweere, J.A., Spangler, R.E., Bohs, L., Palmer, J.D. (1999) Phylogeny and pro-
visional classiﬁcation of the Solanaceae based on chloroplast DNA. In: N. Nee, D.E. Symon,
R.N. Lester and J.P. Jessop (Eds.), Solanaceae IV: Advances in Biology and Utilization. Royal
Bot. Garden, Kew, pp. 111–137.
Olmstead, R.G. and Bohs, L. (2007) A summary of molecular systematic research in Solanaceae:
1982–2006. In: D.M. Spooner, L. Bohs, J. Gionannoni, R.G. Olmstead and D. Shibata (Eds.),
Solanaceae VI: Genomics Meets Biodiversity.Inter.Soc.forHort.Sci.,Brugge,pp.255–268.
Olsen, K.M. and Schaal, B.A. (1999) Evidence on the origin of cassava: Phylogeography of Mani-
Orr, H.A. (2001) The genetics of species differences. Trends Ecol. Evol. 16, 343–350.
Rambo, B. (1951a) O elemento andino no pinhal riograndense. Sellowia 3, 7–39.
Rambo, B. (1951b) A imigrac¸˜
ao da selva higr´
oﬁla no rio Grande do Sul. Sellowia 3, 55–91.
Reis, C., Sajo, M.G. and Stehmann, J.R. (2002) Leaf structure and the taxonomy of Petunia and
Calibrachoa. Braz. Arch. Biol. Techn. 45, 59–66.
Saint-Hilaire, A. (1824) Histoire des plantes les plus remarquables du Br´
esil et Paraguay. Paris,
Sandwith, N.Y. (1926) Pet u n i a fel i p p one i Sandwith. Kew Bulletin 26, 244–245.
Schaal, B.A., Hayworth, D.A., Olsen, K.M., Rauscher, J.T. and Smith, W.A. (1998) Phylogeo-
graphic studies in plants: Problems and prospects. Molec. Ecol. 7, 465–474.
Schaal, B.A., Gaskin, J.F. and Caicedo, A.L. (2003) Phylogeography, haplotype trees, and invasive
plant species. J. Hered. 91, 197–201.
Seehausen, O. (2004) Hybridization and adaptative radiation. Trends Ecol. Evol. 19, 198–207.
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W., Miller, J., Siripun, K.C., Winder, C.T.,
Schilling, E.E. and Small, R.L. (2005) The tortoise and the hare II: Relative utility of 21 non-
coding chloroplast DNA sequences for phylogenetic analysis. Amer. J. Bot. 92, 142–166.
Shetler, S.G. and Morin, N.R. (1986) Seed morphology in North American Campanulaceae. Ann.
Missouri Bot. Garden 73, 653–688.
Sink, K.C. (1984) Petunia. In: K.C. Sink (Ed.), Pet u n i a: Mo n o gra p h s on The o ret i c al and A p p lied
Smith, L.B., Downs, R.J. (1964) Notes on the Solanaceae of Southern Brazil. Phytol. 10, 422–453.
Smith, L.B. and Downs, R.J. (1966) Petunia. In: P.R. Reitz (Ed.), Flora Illustrada Catarinense.
aceas, Santa Catarina, Brazil.Herb
ario Barbosa Rodrigues, Itajai, pp. 261–291.
Smith, T.B., Kark, S., Schneider, C.J. and Wayne, R.K. (2001) Biodiversity hotspots and beyond:
The need for preserving environmental transitions. Trends Ecol. Evol. 16, 431.
Spegazzini, C.L. (1897) Nierembergia patagonica. Revista de la Facultad de Agronom
ıa y Veteri-
naria, La Plata 3, 557.
Steere, W.C. (1931) Pe tun i a p a ro d ii, a new species of the subgenus Pseudonicotiana from
Argentina. Papers Michigan Acad. Sci. 13, 213–215.
Stehmann, J.R. (1987) Petunia exserta (Solanaceae): Uma nova esp´
ecie do Rio Grande do Sul,
Brasil. Napaea 2, 19–21.
Stehmann, J.R., Semir, J., Dutilh, J.H.A. and Forni-Martins, E.R. (1996) Solanaceae. IOPB Chro-
mosome Data. Newsl. Intl. Org. Plant Biosyst. 26–27, 24.
Stehmann, J.R. and Semir, J. (1997) A new species and new combinations in Calibrachoa
(Solanaceae). Novon 7, 417–419.
Stehmann, J.R. and Semir, J. (2001) Biologia reprodutiva de Calibrachoa elegans (Miers)
Stehmann & Semir (Solanaceae). Revista Brasileira de Botˆ
anica 24, 43–49.
Stehmann, J.R. and Semir, J. (2005) New species of Calibrachoa and Petunia (Solanaceae) from
subtropical South America. In: R.C. Keating, V.C. Hollowell and T.B. Croat (Eds.), Festschrift
for William G. Darcy: The Legacy of a Taxonomist. Missouri Bot. Garden Press, Missouri, pp.
Stehmann, J.R. and Bohs, L. (2007) Nuevas Combinaciones en Solanaceae. Darwiniana 45,
Stout, A.B. (1952) Reproduction in Petunia.MemoirsoftheTorreyBot.Club20,1–202.
Strand, A.E., Leebens-Mack, J. and Milligan, B.G. (1997) Nuclear DNA-based markers for plant
evolutionary biology. Molec. Ecol. 6, 113–118.
Tsukamoto, T., Ando, T., Kokubun, H., Watanabe, H., Tanaka, R., Hashimoto, G., Marchesi, E.
and Kao, T. (1998) Differentiation in the status of self-incompatibility among all natural taxa
of Petunia (Solanaceae). Acta Phytotax. Geobot. 49, 115–133.
van der Donk, J .A.W.M. (1974) Gene activ ity and the incompatibility reaction in Petunia.In:H.F.
Linskens (Ed.), Fertilization in Higher Plants.North-HollandPublishingCo.,Amsterdam,pp.
van der Pijl, A. (1982) Principles of Dispersal in Higher Plants,2nd Edn.Springer-Verlag,Berlin.
Villwock, J.A. and Tomazelli, L.J. (1995) Geologia costeira do Rio Grande do Sul. Notas T´
Wat a n a be, H . , A n do, T., I i d a , S., Su z u ki, A. , B u t o, K., T s u kamo t o , T. , Hash i m o to, G. a n d Marc h e s i,
E. (1996a) Cross compatibility of Pet u n ia cultivars and P. axillaris with native taxa of Petunia
in relation to their chromosome number. J. Jap. Soc. Hort. Sci. 65, 625–634.
Wat a n a be, H . , A n do, T., I i d a , S.I . , S u zuki , A . , B uto , K . I ., Tsu k a moto , T. , Koku b un, H. , H a s him o t o ,
G. and Marchesi, E. (1996b) Cross compatibility of Pet u n i a pub e s c ens and P. pygmaea with
native taxa of Petunia. J. Jap. Soc. Hort. Sci. 66, 607–612.
Wat a n a be, H . , A n do, T., N i s h ino, E . , Kok u bun, H . , T s ukam o t o, T., Ha s h i moto , G . a n d Mar c h e si, E.
(1999) Three groups of species in Petunia sensu Jussieu (Solanaceae) inferred from the intact
seed morphology. Amer. J. Bot. 86, 302–305.
Wet t s t ein , R . ( 1 895) S o l anac e a e . In: A. Eng l e r and K. P r a n tl (Ed s . ), Die Nat¨
ilien 4 (3b).VerlagW.Engelmann,Leipzig,pp.4–38.
Wijn ands, D.O . and Bos , J. J. (198 6) Propos al to conse rve 74 36 Petunia with P. nyctaginiﬂora as
Typ . C ons . (Solanaceae). Taxon 35, 748–749.
Wijs man, H.J. W. (1982) O n the inter relatio nship s of c ertai n species o f Petunia.I.Taxonomicnotes
on the parental species of Pet u n i a hyb r i d a.ActaBot.Neerl.31,477–490.
Wijs man, H.J. W. (1983) O n the inter relatio nship s of certai n species o f Petunia. II. Experimental
data: Crosses between different taxa. Acta Bot. Neerl. 32, 97–107.
Wijsman, H.J.W. and Jong J.H. (1985) On the interrelationships of certain species of Pet u n i a.
IV. Hybridization and nomenclatural consequences in the Petunia group. Acta Bot. Neerl. 34,
28 J.R. Stehmann et al.
Wijs man, H.J. W. (1990) O n the inter relat io nship s of certai n species o f Petunia VI. New names for
the species of Calibrachoa formerly included into Petunia (Solanaceae). Acta Bot. Neerl. 39,
Witt mann, D., R adtke , R., Cur e, J .R. and S chiﬁno- Wittmann , M.T. (1990) C oevolv ed repr oductive
strategies in the oligolectic bee Callonychium petuniae (Apoidea, Andrenidae) and three purple
ﬂowered Petunia species (Solanaceae) in southern Brazil. Zeitsch. Zool. System. Evol. 28,