Annals of Botany 86: 323±338, 2000
doi:10.1006/anbo.2000.1188, available online at http://www.idealibrary.com on
SEM and Light Microscope Observations on Fruit and Seeds in Scrophulariaceae from
Southwest Spain and their Systematic Signi®cance
R . J U A N , J . PA S TO R and I . F E R N AÂ N D E Z
Departamento de BiologõÂa Vegetal y EcologõÂa de la Universidad de Sevilla, Apartado 1095, 41080 Sevilla, Spain
Received: 7 February 2000 Returned for revision: 13 March 2000 Accepted: 14 April 2000
Many studies of the morphology and anatomy of fruits and seeds of Scrophulariaceae from Southwest Spain have
been made. The systematic utility of characteristics of these plant structures is discussed in order to determine
relationships among the di€erent genera included in this widely distributed family. The most useful fruit features for
this study were the indumentum, capsule dehiscence and structure of the endocarp, seed-coat ornamentation, and
inner structure of the seeds. In addition, phenetic analysis of 58 characters revealed that several groups of genera in
Scrophulariaceae are closely related on the basis of their fruit and seed features. The phenetic relationships of genera
or groups of genera are discussed. Keys to genera considered in this work, using exclusively fruit or seed characters,
are provided. Lastly, the usual dispersal systems observed in this family are discussed.
# 2000 Annals of Botany Company
Key words: Fruit, seed, morphology, anatomy, Scrophulariaceae, phenogram, SEM, pericarp, dehiscence,
indumentum, seed-coat.
I N T RO D U C T I O N
The largest genera, in terms of number of species, in the
cosmopolitan family Scrophulariaceae s.l., described by
Jussieu (1789), are mainly distributed throughout the temperate areas of the northern hemisphere (Heywood, 1985).
The study area, SW Spain, is noted for its ¯oristic diversity,
and the family Scrophulariaceae is very well represented with
99 taxa (excluding hybrids) belonging to 19 genera. The
classi®cation of ValdeÂs (1987) in Flora Vascular de AndalucõÂa
occidental is adopted, due to its total correspondence with
the study area, where this family is represented by the
traditional subfamilies Verbascoideae, Scrophularioideae
and Rhinanthoideae (Table 1), which are usually di€erentiated by aestivation of petals and by leaf disposition.
Plants of the family Scrophulariaceae are herbs or small
shrubs, a few trees, high shrubs or lianas. Some taxa are
hemiparasitic or holoparasitic, although the parasites in
this family are generally not host speci®c. The family has
simple, alternate or opposite leaves. Its main characteristics
are an in¯orescence which is racemose or cymose, widely
variable in each genus; ¯owers hermaphrodite, pentamerous, and occasionally tetramerous; corolla zygomorphic or
nearly actinomorphic, often bilabiate, sometimes with spur
or basal hump; calyx usually with four-®ve lobes; didynamous stamens, sometimes with ®ve or two (-three) stamens;
ovary superior with two united carpels and two locules,
often with numerous ovules on two axile placentas; style
single; fruit capsule, with various types of dehiscence; and
seeds widely variable.
The limits of the Scrophulariaceae may sometimes be
confused due to the existence of some closely related families such as Bignoniaceae, Nelsoniaceae, Orobanchaceae,
Acanthaceae and Globulariaceae. Stace (1985) indicated the
0305-7364/00/080323+16 $35.00/00
absence of a clear separation between Scrophulariaceae and
Orobanchaceae, which are sometimes fused into a single
family. Moreover, Dahlgren (1980) and Takhtajan (1997)
included Orobanchaceae and Nelsoniaceae in Scrophulariaceae. However, other authors consider Orobanchaceae to
be a di€erent and more advanced family, especially with
respect to parasitism, probably originating from the subfamily Rhinanthoideae (Scrophulariaceae) (Hutchinson,
1969; Cronquist, 1981).
T A B L E 1. Classi®cation followed in Scropulariaceae for the
present study (ValdeÂs, 1987)
Subfamilies
Tribes
Genera
Verbascoideae
Verbasceae
Verbascum
Scrophularioideae
Scrophularieae
Antirrhineae
Scrophularia
Anarrhinum
Antirrhinum
Chaenorrhinum
Cymbalaria
Kickxia
Linaria
Misopates
Gratiola
Rhinanthoideae
Sibthorpieae
Digitaleae
Gratioleae
Veroniceae
Rhinantheae
Sibthorpia
Digitalis
Erinus
Veronica
Bartsia
Bellardia
Odontites
Parentucellia
Pedicularis
# 2000 Annals of Botany Company
324
Juan et al.ÐFruits and Seeds of Scrophulariaceae
Chant (1985) commented on the presence of common
characters between the families Acanthaceae and Scrophulariaceae, such as the possession of irregularly pentamerous
¯owers, a reduced number of stamens and a superior ovary
with two carpels; however, not all authors are in agreement
with this opinion. Cronquist (1981) explains that these
similarities are not enough to join the two families, although
the same author recognized that the limits are sometimes
arbitrary. Takhtajan (1980) also included the family Globulariaceae in Scrophulariaceae. However, in previous work
(Takhtajan, 1969) the former taxon was considered a
separate family, in agreement with other authors. Cronquist
(1981) indicated the possible connection between both
families through the tribe Manuleae (Scrophulariaceae).
The anities among these groups have led to certain
genera being considered to belong to one or other family
depending on the characters emphasized by di€erent
authors. For example, genera such as Lathraea, Buchnera
or Hyobanche can be found in the literature included
in Scrophulariaceae or Orobanchaceae (Minkin and Eshbaugh, 1989). The taxa of Orobanchaceae (holoparasites)
and the parasitic taxa of Scrophulariaceae coincide in most
of their ¯oral features, although the families can usually be
distinguished by the placentation and the number of
carpels. Genera such as Paulownia have been included in
Scrophulariaceae (Hutchinson, 1969) or in Bignoniaceae
(Takhtajan, 1980; Cronquist, 1981).
The diculties in delimiting the di€erent possible family
groups motived the search for usable characters, and several
comparative studies were made. Boeshore (1920) studied
the morphological continuity between Scrophulariaceae
and Orobanchaceae based on di€erent characters (roots,
leaves, in¯orescences, ¯owers). CreÂte (1955) examined the
possible utility of some embryological features in the
systematics of Orobanchaceae and some allied families
such as Scrophulariaceae, Gesneriaceae and Bignoniaceae.
Later, Musselman and Mann (1976) compared the seed
morphology of Orobanchaceae and Scrophulariaceae. Other
authors attempted to delimit the Scrophulariaceae from the
Bignoniaceae based on ¯oral anatomy and placentation
(Armstrong, 1985). Palynological comparative studies were
also carried out on Orobanchaceae and Rhinanthoideae
(Minkin and Eshbaugh, 1989).
Recent molecular phylogenetic investigations on the
Scrophulariaceae, Orobanchaceae or Bignoniaceae are providing new data about their delimitation. Young et al.
(1997) included the hemiparasites of Scrophulariaceae within the Orobanchaceae. Olmstead and Reeves (1995) and
Olmstead et al. (1998) indicated the polyphyly of the
Scrophulariaceae. Finally, Spangler and Olmstead (1999)
included Paulownia, which was previously considered to
belong to Scrophulariaceae or Bignoniaceae, in Paulowniaceae.
Studies on the morphology and anatomy of fruits and
seeds have been useful to support the delimitations of
individual or groups of taxa. With respect to the family
Scrophulariaceae, authors have considered di€erent morphological and anatomical aspects e.g. Chatin (1874),
Meunier (1897), Yamazaki (1957), Chuang and Heckard
(1972, 1983), Fernandes (1973), Falcao Ichaso (1978),
Canne (1979, 1980), Elisens and Tomb (1983), Elisens
(1985a,b), Speta (1986), Sutton (1988) and Krause and
Weber (1990). However, none of these authors studied all
fruit and seed characters at a family level. Such a study is
necessary to increase our knowledge not only of seed variability in Scrophulariaceae, but also of fruit features, to
which many authors have paid less attention.
In the present work we analyse and discuss fruit and seed
characters in the context of the family Scrophulariaceae in
all the genera present in the southwest of Spain. Detailed
studies of genera have been published separately (Juan et al.,
1994, 1995, 1996a,b,c,d, 1997a,b,c, 1998a,b,c, 1999a,b,c,d).
Thus, the aims of this paper are to: (a) o€er a global view
on the systematic utility of the characters derived from the
fruit and seed studies; (b) discuss the anities of the genera
based on these characters; (c) prepare fruit and seed keys
(Appendices 1 and 2) to aid identi®cation within the
examined genera; and (d) comment on the possible and
most frequent dispersion strategies according to the features
observed.
M AT E R I A L S A ND M E T H O D S
Material used for this study was collected from wild
populations as well as from herbarium specimens. Collectors and localities are shown in Appendix 3. Voucher
specimens of the plants are deposited in the Herbarium of
the Departamento de BiologõÂ a Vegetal y EcologõÂ a de la
Universidad de Sevilla, Spain.
For scanning electron microscopic observation, fruits
and seeds were dehydrated in an acetone series, critical
point dried using carbon dioxide and, together with dry
seeds, were mounted directly on stubs using double-side
adhesive tape, and sputter-coated with gold. Observations
were made in a Philips LX-20 Autoscan SEM. Terminology
of seed-coat surface sculpturing basically follows Stearn
(1992) and Font Quer (1993).
For anatomical investigations, mature fruits and seeds of
FAA-preserved material were rinsed in 70 % ethanol prior
to dehydration. Dehydration and embedding were carried
out by the tertiary butyl alcohol method (Johansen, 1940),
in®ltrated with paran and sectioned at a thickness of
8±10 mm. The sections were then attached to glass slides,
stained with safranin and fast green solutions and permanently mounted.
To study epidermal features using light microscopy, some
capsules were ®xed in FAA and soaked in lactic acid to
facilitate the separation of the epidermis. Hairs were drawn
by means of a camera lucida.
Finally, a phenetic study of 19 genera of Scrophulariaceae was made using 58 qualitative characters (Table 2).
NTSYS-pc (Rohlf, 1990) was used to produce a phenogram
using the unweighted pair-group method with an arithmetic
average (UPGMA) from the data matrix (Table 3).
R E S U LT S A N D D I S C U S S I O N
The results of the present work display the utility of fruit
and seed characters for distinguishing the examined genera
in Scrophulariaceae. These kinds of characters were used
Juan et al.ÐFruits and Seeds of Scrophulariaceae
T A B L E 2. Morphological and anatomical characters used in
phenetic analysis of Scrophulariaceae genera
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
Capsule with dorsi-ventral symmetry
Capsule with di€erent symmetry
Dehiscence septicidal
Dehiscence loculicidal
Dehiscence septicidal-loculicidal
Dehiscence foraminal
Abaxial loculus opening by two porus
Porus opening by teeth
Porus elongated with parallel-sided
Porus opening by regular valves
Porus opening by irregular valves
Porus opening by circumcissile split
Capsule glabrous
Capsule with indumentum
Capsule with indumentum adpressus
Capsule with indumentum not adpressus
Capsule with glandular hairs
Capsule with eglandular hairs
Capsule with branched hairs
Glandular hairs with unicellular head
Smooth hairs
Papillate hairs
Verrucate hairs
Eglandular hairs with enlarged base
Capsule compressed
Median length of capsule 44 mm
Median length of capsule 44 mm
Seeds up to 50 per capsule
More than 150 seeds per capsule
Endocarp scarcely ligni®ed
Mesocarp with two di€erent regions
Cells of seed epidermis with membranous tangential walls
Seeds cristate
Seeds tuberculate
Seeds reticulate
Seeds alveolate
Seeds with alveoli arranged in longitudinal rows
Seeds with multicellular ridges
Seeds with longitudinal ridges
Seeds with transverse ridges
Seeds with irregular ridges
Seeds with ridges anastomosed
Seeds with epicuticular waxes
Median length of seeds 40.6 mm
Median length of seeds 40.6 mm
Seed with concave ventral face
Endosperm ruminate
Endothelium reduced to a ®lamentous layer
Epidermal cells of seeds with scalariform thickening
Epidermal cells of seeds with helicoidal thickening
Epidermal cells of seeds with reticulate thickening
Epidermal cells of seeds with perforate thickening
Epidermal cells of seeds with alveolate thickening
Seed-coat only formed by epidermis
Seed-coat formed by epidermis and endothelium
Seed-coat formed by epidermis, hypodermis and endothelium
Embryo 51/3 in relation to endosperm
Embryo 41/2 in relation to endosperm
previously by authors studying a representative number of
genera of Papilionaceae (Gunn, 1984, 1991). Consequently,
fruit and seed characters could be the basis of a classi®cation at di€erent levels of taxa. The natural or arti®cial
nature of this classi®cation is a subject that will only be
clari®ed when much more information about the anatomy
and morphology of these structures is available.
325
Mechanisms of dehiscence
Among the examined genera it is possible to establish
four groups: (1) septicidal (Verbascum, Scrophularia and
some Digitalis species); (2) foraminal (Antirrhinum, Misopates, Anarrhinum, Linaria, Kickxia, Chaenorrhinum and
Cymbalaria, all the studied genera of the tribe Antirrhineae); (3) loculicidal (Sibthorpia, some Veronica species,
and the tribe Rhinantheae, represented in the study area by
Pedicularis, Bartsia, Bellardia, Parentucellia and Odontites);
and (4) loculicidal-septicidal or vice versa (Gratiola, Erinus,
and some species of Veronica and Digitalis (Fig. 1).
The dehiscence mechanisms in capsules of Scrophulariaceae have a high systematic value, and they have sometimes been used in supraspeci®c classi®cations. Within each
established group, it is possible to distinguish the di€erent
genera by several fruit characters such as symmetry, size,
shape, apex, indumentum, etc. Other more detailed characters such as hair types or cellular morphology of the
surface have been of great utility at the infrageneric level,
allowing us to identify most of the studied species.
Indumentum diversity of capsules
The capsule epidermis was highly diverse in this family
(Juan et al., 1995, 1996a,b, 1997a,b,c, 1998a,b,c, 1999a,b).
The utility of this feature had previously been shown for the
Papilionaceae (Dave and Bennet, 1989) or at the speci®c
level in the genus Antirrhinum (Doaigey and Harkiss, 1991).
The diversity of hair types in Scrophulariaceae was made
evident by Raman (1987, 1989a,b, 1990a,b, 1991) mainly
studying the corollas of several genera belonging to this
family. This author claimed that hair features constitute an
important character in plant systematics, and could be
useful in the identi®cation of genera, species and hybrids. In
the studied taxa from SW Spain, we observed a higher
variability in glandular hairs than in eglandular ones
(Fig. 2), which is a useful character in the identi®cation of
the di€erent taxa. Admittedly, the number of genera with
glabrous capsules was small (Scrophularia, Cymbalaria,
Gratiola and Pedicularis, plus some species of Linaria,
Veronica and Parentucellia). Papillae were not very abundant, being present only in some species of Verbascum and
Chaenorrhinum.
Among the eglandular hairs, unicellular ones with enlarged bases are of the most characteristic (Fig. 2H, I). This
kind of eglandular hair has only been observed on fruits of
genera of the tribe Rhinantheae such as Bartsia, Bellardia,
Odontites and Parentucellia (Juan et al., 1996b, 1998b).
Sibthorpia also shows a very distinct hair type, with acute
apex, cellular junctions clearly marked, and a papillose
surface (Fig. 2G), giving an overall robust appearance with
respect to the size of the capsules which are less than 2 mm
long. In the remaining genera, eglandular and glandular
hairs may coexist, as in some species of Antirrhinum,
Veronica and Chaenorrhinum (Fig. 2J), but eglandular hairs
are less abundant in all cases. These eglandular hairs are
only distinguished from each other by the possession of a
smooth, granulose or verrugose surface (Juan et al., 1996a,
1997a,b).
326
Juan et al.ÐFruits and Seeds of Scrophulariaceae
T A B L E 3. Data matrix for phenetic analysis of Scrophulariaceae genera
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
A
B
C
D
E
F
G
H
I
J
K
L
M
N
O
P
Q
R
S
0
1
1
0
0
0
9
9
9
9
9
9
0
1
0
1
1
0
1
0
1
0
0
0
0
1
1
1
1
0
1
1
0
0
0
1
1
9
9
9
9
9
0
0
1
0
1
1
1
0
0
0
0
0
1
0
0
0
0
1
1
0
0
0
9
9
9
9
9
9
1
0
9
9
9
9
9
9
9
9
9
9
0
0
1
1
1
0
1
1
0
0
0
1
1
9
9
9
9
9
0
1
1
0
1
0
1
0
0
0
0
0
1
0
0
0
1
0
0
0
0
1
1
1
0
0
0
0
0
1
0
1
1
1
0
1
1
0
0
0
0
0
1
0
1
0
0
0
1
0
0
0
9
1
1
0
0
1
1
1
1
0
0
0
0
1
0
0
0
0
0
1
0
0
1
0
0
0
0
1
1
1
0
0
0
0
0
1
0
1
1
0
0
0
0
0
1
9
0
0
1
0
1
0
0
0
0
0
0
0
9
9
9
9
9
9
1
0
1
1
0
0
0
1
0
0
0
0
0
1
0
0
0
1
0
0
0
1
0
0
1
0
0
0
0
1
0
1
1
0
0
1
1
0
0
9
0
1
0
0
0
0
0
0
0
1
0
0
9
9
9
9
9
9
0
1
1
0
0
0
0
1
0
0
0
0
0
1
0
0
1
1
0
0
0
1
0
1
0
1
0
0
1
1
0
1
1
0
0
1
1
0
0
9
0
1
1
1
1
0
0
0
1
0
0
1
0
1
0
1
0
0
0
1
1
1
0
0
0
1
0
0
0
0
1
1
0
0
1
1
0
0
0
1
0
1
0
0
0
1
0
1
0
1
1
1
0
1
1
1
0
0
0
1
1
0
1
0
0
0
1
0
0
0
9
1
1
0
0
0
1
1
0
0
0
0
0
1
0
0
0
0
0
1
0
0
0
1
0
0
0
1
0
0
0
0
0
1
0
1
0
1
1
1
0
1
1
0
1
0
0
1
0
1
0
0
0
0
1
1
0
1
0
1
0
0
1
0
0
0
1
0
0
0
0
1
0
0
0
0
0
1
0
0
0
1
0
0
0
1
0
0
0
0
1
0
1
0
9
9
9
9
9
9
9
9
9
9
0
0
1
1
0
0
0
0
1
0
0
0
9
1
0
0
1
0
1
0
1
0
0
0
0
1
0
0
0
0
0
1
0
0
0
1
0
0
1
0
9
9
9
9
9
9
1
0
9
9
9
9
9
9
9
9
9
9
0
0
1
0
0
0
0
1
0
0
1
0
9
9
9
9
9
9
0
0
1
0
0
9
0
0
1
0
0
1
0
0
0
1
0
1
0
1
0
0
9
9
9
9
9
9
0
1
0
1
0
1
0
0
0
1
0
0
1
1
0
1
0
1
0
1
0
0
1
0
9
9
9
9
9
9
0
1
0
1
0
0
0
0
1
0
0
0
1
0
1
0
0
1
1
0
1
0
9
9
9
9
9
9
0
1
0
1
1
1
0
1
1
0
0
0
0
0
1
0
1
0
0
1
0
0
1
0
9
9
9
9
9
9
0
1
1
0
0
0
0
0
0
1
1
0
1
0
0
0
0
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0
0
1
0
9
9
9
9
9
9
0
1
0
1
1
0
0
1
1
0
0
9
0
1
0
1
0
0
0
1
0
0
1
0
9
9
9
9
9
9
0
1
0
1
0
0
0
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1
0
0
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1
0
0
0
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0
1
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0
9
9
9
9
9
9
1
1
0
1
1
1
0
1
1
1
1
0
1
1
1
1
0
1
0
1
1
0
1
1
0
1
0
1
0
0
0
1
1
1
0
0
9
9
9
9
9
1
1
0
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9
9
9
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9
9
1
0
9
9
9
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9
9
9
9
9
9
0
0
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1
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0
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9
9
9
9
9
9
0
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9
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9
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9
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±
±
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0
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9
9
9
9
9
9
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1
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0
1
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1
1
0
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1
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1
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0
0
9
0
1
0
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0
0
9
9
9
9
9
9
1
1
1
0
0
1
0
9
1
0
0
1
0
0
1
0
1
0
0
1
0
0
1
0
9
9
9
9
9
9
0
1
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
1
0
1
0
0
9
9
9
9
9
9
0
1
1
0
0
1
0
9
1
0
0
1
1
1
1
1
0
0
0
1
1
0
0
0
9
0
1
0
0
0
0
0
1
0
0
0
0
0
1
0
0
0
0
1
0
0
A, Verbascum; B, Scrophularia; C, Antirrhinum; D, Misopates; E, Anarrhinum; F, Linaria; G, Chaenorrhinum; H, Kickxia; I, Cymbalaria; J,
Gratiola; K, Sibthorpia; L, Digitalis; M, Erinus; N, Veronica; O, Pedicularis; P, Bartsia; Q, Bellardia; R, Parentucellia; S, Odontites. (0, absent
characters; 1, present characters; 9, missing characters; Ð, no data available).
Juan et al.ÐFruits and Seeds of Scrophulariaceae
327
F I G . 1. Dehiscence types (based on and modi®ed from Sutton, 1988). A, Septicidal. B±J, Foraminal. K, Septicidal and loculicidal. L, N, P,
Loculicidal. M, Septicidal and partially loculicidal. O, Loculicidal and partially septicidal.
Some authors, such as Bolliger (1985) and Raman
(1990a), indicated the frequent presence in the Scrophulariaceae of glandular hairs with a head composed of
longitudinal or transverse cells. Despite this, and although
glandular hairs displayed higher variability in this study,
only longitudinal divisions were observed among the
examined genera (Fig. 2B, C, E, F). These were especially
frequent in the tribe Antirrhineae (Antirrhinum, Misopates,
Linaria, Chaenorrhinum and Kickxia). The hairs are slightly
di€erent in the genus Verbascum (Juan et al., 1997c) where
they are often small (5100 mm long, with a large head
relative to the stalk size (one or two cells) (Fig. 2B).
Glandular hairs with unicellular heads are also abundant in
other genera, the most characteristic being those of some
species of Linaria, which possess a globular or semiglobular
head, and a stalk composed of various cells which are
shorter at the apex of the hair (Juan et al., 1999a) (Fig. 2D).
Those present in Digitalis and Veronica (Fig. 2J) are clearly
di€erent, having an obovoid head, and stalk with larger
cells. The indumentum of several species of Verbascum,
composed of branched hairs, is unique among the studied
genera (Fig. 2A). However, according to Cantino (1990),
this hair type is present in some genera of Scrophulariales,
although it is not common in the largest families.
Fruit anatomy
Anatomy of the endocarp of the capsule is variable. For
instance, the capsule walls of Antirrhinum, Verbascum, and
Scrophularia (Juan et al., 1996a, 1997c, 1999d) manifested a
high degree of complexity, expressed by the high number of
cellular layers with di€erent orientation and morphology
(Fig. 3A, B). This complexity was also observed in some
studies of the pericarp structure e.g. in the Boraginaceae
(Hilger, 1989) and Anacardiaceae (Wannan and Quinn,
1990). In spite of this, the most common case is an endocarp consisting only of two cellular layers of di€erent size
and ligni®ed to a greater or lesser extent, as occurs in
Linaria and Digitalis (Fig. 3C). The most extreme case was
observed in the genus Veronica, in which the endocarp is
scarcely ligni®ed (Fig. 3E).
The mesocarp and the epicarp are not suciently
distinguishable to enable di€erentiation among the examined genera in this family. However, in some species of
Verbascum and Scrophularia the mesocarp shows two di€erent regions resulting from size di€erences among the cells
(Fig. 3B).
Taking into account the dehiscence and anatomical
features of the capsules as a whole, a clear relationship
between the sets of characters is observed. In septicidal
dehiscence, loculi are separated by tension caused during
the drying phase by the di€erent orientation of the cellular
layers (e.g. Verbascum, Scrophularia). In capsules with
foraminal dehiscence, the endocarp is often simpli®ed in the
porus area, where the orientation of the cell layers determines the direction in which valves or teeth are folded (e.g.
Antirrhinum, Linaria, Misopates, Anarrhinum), or a circular
abscission line is located in the pore area (e.g. Kickxia,
Chaenorrhinum). In some genera with loculicidal dehiscence
such as Sibthorpia or Veronica, the abscission tissue in the
middle of each loculus is clearly evident. In addition, a
cohesion tissue can be found in some species of Veronica,
which contributes to the e€ective aperture in these capsules
(Juan et al., 1997a).
Number, shape and size of the seeds
The number of seeds produced per capsule could be
considered a diagnostic character, although at the generic
level the range of variation is so high that it is very dicult
to establish any relationship. All the studied species of
Digitalis, Misopates, Antirrhinum, Bellardia and Parentucellia show a high number of seeds (4150); this is also
found in some species of Verbascum, Scrophularia, Linaria
328
Juan et al.ÐFruits and Seeds of Scrophulariaceae
F I G . 2. Scanning electron micrographs of trichomes on capsules of Scrophulariaceae. A, Branched hair. B-F, Glandular hairs. G, H, Eglandular
hairs. I, J, Glandular and eglandular hairs. A, Verbascum simplex. B, V. barnadesii. C, Veronica hederifolia subsp. triloba. D, Linaria saxatilis.
E, Misopates orontium. F, Antirrhinum graniticum subsp. onubensis. G, Sibthorpia europaea. H, Parentucellia viscosa. I, Bellardia trixago.
J, Kickxia spuria. Bars ˆ 100 mm (A, E, G-I); 50 mm (J, F); 20 mm (B-D).
and Chaenorrhinum. In contrast, Bartsia (according to
Bolliger and Molau, 1992), Kickxia, Cymbalaria, Erinus,
Pedicularis, Odontites, Veronica (Juan et al., 1996b,c, 1997a,
1998c), and some species of other genera, have fewer seeds
per capsule (550).
Seed shape and size is very heterogeneous, even within
the same species. In general, and according to Chuang and
Heckard (1983), the shape of the seed is directly related to
the insertion of these in the fruit. In other words, seeds with
lateral insertion are more or less reniform, while seeds with
terminal insertion are ovoids, fusiforms or prismatics. Some
of the examined genera, such as Linaria and Veronica,
possess reniform or cyathiform seeds, with lateral or ventral
insertion, while in other genera with terminal insertion, e.g.
Digitalis and Verbascum, seeds are more or less prismatic in
shape. The shape of the seed also changes with its relative
position in the capsule. Seed size is also a variable feature,
although seeds are often small (3.1±0.3 mm in length). The
largest seeds are found in some taxa of Pedicularis or
Linaria while the smallest seeds are found in Parentucellia
and Bellardia.
Seed morphology
According to Molau (1990), the morphology of the seedcoat provides a set of useful characters, demonstrated in
Juan et al.ÐFruits and Seeds of Scrophulariaceae
329
F I G . 3. Sections of mature fruits and seeds of Scrophulariaceae. A±C, E, Cross section of mature pericarp. D, F, O, Cross section of mature seed.
E, G±N, Cross section of mature seed-coat. A, Scrophularia sambucifolia. B, S. lyrata. C, Linaria tartessiana. D, L. triphylla. E, Veronica
cymbalaria. F, Gratiola linifolia. G, Veronica agrestis. H, Sibthorpia europaea. I, Scrophularia oxyrhyncha. J, Verbascum rotundifolium subsp.
haenseleri. K, Parentucellia viscosa. L, Cymbalaria muralis. M, Linaria amethystea subsp. multipunctata. N, Anarrhinum bellidifolium. O,
Sibthorpia europaea. Bars ˆ 100 mm (A±C, E±J, L±O); 50 mm (D, K).
several tribes and subtribes of Scrophulariaceae, showing a
constancy in the types observed mainly within the subtribes.
Features of the tangential wall in the epidermal cells of
the seeds of the studied genera allow us to establish two
groups. In the ®rst group this wall is membranous
(Verbascum, Scrophularia, Gratiola, Sibthorpia, Digitalis,
Erinus, Bartsia, Bellardia, Parentucellia, Odontites and
Pedicularis (Fig. 4B, G±J), and in the second group of
genera, this structure is thickened (Antirrhinum, Anarrhinum, Misopates, Chaenorrhinum, Kickxia, Linaria, Cymbalaria and Veronica (Fig. 4A, C±F, K).
330
Juan et al.ÐFruits and Seeds of Scrophulariaceae
F I G . 4. Scanning electron micrographs of Scrophulariaceae seeds. A, Seed winged. B, Alveolate seed. C±F, Cristate seeds. G, J, Reticulate seeds.
H, Seed cristate-winged. I, Reticulate seed treated with critical point dried. K, Surface with epicuticular waxes. A, Linaria amethystea subsp.
multipunctata. B, Verbascum dentifolium, C, Chaenorrhinum rubrifolium. D, Antirrhinum graniticum subsp. boissieri. E, Cymbalaria muralis.
F, Linaria spartea. G, Gratiola ocinalis. H, Bellardia trixago. I, Digitalis purpurea subsp. mariana. J, Sibthorpia europaea. K, Chaenorrhinum
macropodum subsp. degenii. Bars ˆ 500 mm (A); 200 mm (B±H); 50 mm (I±K).
Among the studied genera, only Verbascum (tribe
Verbasceae) and Scrophularia (tribe Scrophularieae) have
seeds with longitudinal rows of alveoli (Fig. 4B). In
agreement with Sutton (1988), in the tribe Antirrhineae
seeds with multicellular ridges predominate, and these vary
in number, shape, margins and orientation (Fig. 4C±F). In
general, the ridges are oriented parallel to the main axis of
the seed, but transverse ridges have occasionally been
observed (Linaria, sect. Versicolores). Reticulate seed-coats
have been observed in several genera belonging to di€erent
tribes, such as Gratioleae (Gratiola), Sibthorpieae
(Sibthorpia), Digitaleae (Digitalis, Erinus), Rhinantheae
(Parentucellia, Pedicularis), all except for Gratiola belonging to the subfamily Rhinanthoideae (Fig. 4G, I, J).
The genera Bartsia, Bellardia and Odontites possess
longitudinal ridged or winged seeds (Fig. 4H). However,
these structures are quite di€erent from those present in the
tribe Antirrhineae, because in the former group these are
formed by extension of the cells, and are not multicellular
structures as in Antirrhineae.
Juan et al.ÐFruits and Seeds of Scrophulariaceae
Morphologically, the seeds of some Scrophulariaceae are
very similar to those of Orobanchaceae, as was previously
pointed out by Boeshore (1920), and Musselman and Mann
(1976). More recently, Zhi-Yun (1988, 1990) pointed out
the great similarity between seeds of Orobanche and Cistanche and those from some genera of Scrophulariaceae.
According to Molau (1990), some genera of Orobanchaceae
display seed morphologies of those of the subtribe Euphrasinae in the Scrophulariaceae. This author claimed that a
revision of the generic limits within the tribe Rhinantheae is
necessary, and that the possible polyphylletic origin of the
Orobanchaceae could probably be demonstrated. Palynological studies in Orobanchaceae and Rhinanthoideae
(Minkin and Eshbaugh, 1989) indicated more di€erences
between Rhinanthoideae and Antirrhinoideae than between
Rhinanthoideae and Orobanchaceae. Based on molecular
data, Young et al. (1997) consider the monophyly of the
parasites (hemiparasitic Scrophulariaceae and holoparasitic
Orobanchaceae).
Seed anatomy
The most usual feature observed during analysis of the
inner structure of the seed was a seed-coat composed of the
epidermis and the endothelium, as occurs in Verbascum,
Scrophularia, Sibthorpia and Parentucellia (Fig. 3H±J).
Nevertheless, in some Veronica species that structure is only
formed by the epidermis (Fig. 3G), although in some cases
it may be termed by a combination of the epidermis,
hypodermis and endothelium, as occurs in Antirrhinum,
Misopates, Cymbalaria and Odontites (Fig. 3L±N). In some
cases, the hypodermis can contribute to the formation of
prominences in the seed-coat surface, as occurs in
Anarrhinum and Chaenorrhinum (Fig. 3N). Only the genera
Scrophularia and Verbascum show a ruminate endosperm
where each lobe corresponds to that of the endothelial cells
surrounding it (Fig. 3I, J). This feature was observed by
Bhandari et al. (1976) for Scrophularia himalensis. The
endothelium in Verbascum consists only of a single
®lamentous layer, while in Scrophularia this layer is not
®lamentous, and is thus a useful character to distinguish the
seeds of the two genera.
Frequently the epidermal cell walls of Scrophulariaceae
seeds are reinforced with secondary thickenings (Elisens,
1985a; Sutton, 1988). Among the examined genera,
Verbascum and Scrophularia display scalariform thickenings in the epidermis. Remaining genera, except Veronica,
have a reinforced epidermis, although these thickenings
may often be absent in the outer tangential wall. The
possession of an epidermis with thickening is not exclusive
to this family, being frequent in Orobanchaceae (Zhi-Yun,
1988). According to Barthlott (1981), these secondary thickenings in the epidermal cells could have a high systematic
value, and could characterize genera or subfamilies. In this
study it was observed that genera of the tribe Antirrhineae
display helicoidal thickenings (Fig. 3L, N) in other genera
such as Sibthorpia, Bellardia or Odontites (Juan et al.,
1996b, 1999b) these are reticulated, while in Digitalis (except
for D. obscura) the walls are symmetrically perforated (Juan
et al., 1998a).
331
According to Martin (1946), the embryo is linear and
slightly displaced to one of the poles. However, in the
species examined the embryo and endosperm usually represented approximately the same volume (Fig. 3D), although
the embryo can be smaller as occurs in Sibthorpia,
Pedicularis and some Veronica species (Fig. 3O) or occupy
the greater part of the volume available, as occurs in
Gratiola (Fig. 3F). With respect to the endosperm, the
thickened outer wall of the cells form the limit of the
endothelium. This fact is clearly observable mainly in those
species in which the seed-coat is composed only of the
epidermis; in these cases the endosperm cells contribute to
the protection of the embryo (Veronica).
Epicuticular waxes were observed in the genera
Antirrhinum, Misopates, Chaenorrhinum and Cymbalaria
(Fig. 4K). These kinds of deposits have also been studied in
Cordylanthus (Scrophulariaceae) (Chuang and Heckard,
1972) and Orobanchaceae (Musselman and Mann, 1976).
Apart from the composition of these substances, the distributions and orientations of these secretions on the di€erent
surfaces could be of systematic importance. In general,
epicuticular secretions display a high variability between
related species, although these di€erences could be related to
environmental conditions (Barthlott, 1981). Of the genera
examined possessing epicuticular waxes, we did not observe
di€erences at the speci®c or generic level; the variable
amount of these materials is only of interest with respect to
the considered species. Nevertheless, Sutton (1988) indicated, in Chaenorrhinum, the possible importance of this
character at infrageneric level.
Adaptative values from seed and fruit features
In the present study we have made evident the taxonomic
value that seed and fruit characters can have in the family
Scrophulariaceae. However, it is much more dicult to
understand their adaptative values. Despite this, several
studies have been carried out (e.g. Barthlott, 1981; Elisens
and Tomb, 1983; Telenius and Torstensson, 1989). Elisens
and Tomb (1983) suggested a possible adaptation to
dispersion by water or wind in many genera of Antirrhinae,
due to the presence of expanded epidermal cells that
remain full of air in mature seeds. This kind of cell has also
been observed in Antirrhinum, Anarrhinum, Misopates and
Chaenorrhinum. The wing observed in many species of
Linaria is a clear adaptation to dispersion by wind. The
eciency of this structure was pointed out by Telenius and
Torstensson (1989) studying Spergularia. A reticulated seed
coat has often been related to water dispersion due to these
seeds having the capacity to trap air, thus increasing buoyancy (Van der Pijl, 1982). This fact has been tested in some
genera such as Digitalis and Sibthorpia (Juan et al., 1998a,
1999b).
The presence of a surface with more or less developed
protuberances seems to have adaptative advantages for
these seeds. For instance, Barthlott (1981) suggested that
non-smooth seeds are much less likely to be contaminated
by small particles or pathogens than smooth ones. The
rough surface could also help to control the temperature in
sunlight. Finally, the high hydration ability exhibited by
332
Juan et al.ÐFruits and Seeds of Scrophulariaceae
some genera studied, mainly Verbascum, Scrophularia,
Gratiola, Sibthorpia, Digitalis, Erinus and Parentucellia, is
also of interest. Another phenomenon observed in these
seeds during this hydrated phase is the increased ability to
®x small particles that could create a microclimate for the
seeds to avoid drying damage, as was indicated by Hedge
(1970) for some species of Salvia. The increase in adhesive
capacity could be related to the production of mucilaginous
substances, as was previously indicated by Swarbrick (1971)
and Grubert (1974) for Scrophulariaceae, among other
families. These mucilaginous materials could also be related
to germination processes, as suggested by Gutterman et al.
(1967) for Blepharis persica (Acanthaceae).
With respect to the dispersal system displayed by the
examined genera, passive dispersion is predominant, due
principally to dehiscence type and the arrangement of capsules. Environmental variables such as rain, animals, or, in
general, the wind, produce oscillation of the branches
favouring dispersal seeds from the fruit. Furthermore, it is
important to distinguish between genera that tend to spread
their seeds away from the place of origin (telechory), from
those other genera that disperse their seeds close to their
origin (atelechory). The ®rst group consists of Verbascum,
Scrophularia, Antirrhinum, Misopates, Anarrhinum, Linaria,
Gratiola, Digitalis, Erinus, Bartsia, Bellardia, Parentucellia,
Odontites and some species of Chaenorrhinum and Veronica. The second group is mainly formed by Kickxia,
Cymbalaria, Sibthorpia, Pedicularis and some species of
Chaenorrhinum and Veronica.
Within the former group, some genera such as Bellardia
and Parentucellia have small seeds, similar to those of some
Orobanchaceae or Orchidaceae, and known as `dust-seeds'.
Decreasing seed size, and increasing of the stem length both
tend to increase the dissemination (Matlack, 1987), as has
occurred in some genera such as Digitalis, Verbascum, Antirrhinum or Scrophularia, where, in addition, the number of
seeds per capsule is often high. The stem in Bellardia and
Parentucellia is shorter compared with the above mentioned
genera, although the size of the seeds is also smaller and
thus, these two factors could compensate for each other.
Thompson and Rabinowitz (1989) correlated the size of
the seed with the size of the plant, the initial hypothesis
being that `big plants must have big seeds'. However, these
authors included the Scrophulariaceae as one of the exceptions (among others), and related this fact to the high
incidence of hemiparasitism in this family. Among the
genera of the ®rst group, Linaria is the only genus in which
xerochasy has been observed, a very sophisticated mechanism that, according to Sutton (1988), will favour the dispersion of seeds during drying periods, and so giving a
longer permanence in the air to reach more distant places.
The genera considered in the second group usually display isolated capsules, with more or less elongated and
¯exible peduncles, the capsules being situated near to the
substratum, and atelechory being favoured. Pedicularis is
the unique exception to this rule, although the short stem of
the plant and the relatively large size of the seeds contribute
to the short dispersion. Thompson and Rabinowitz (1989)
indicated the possible exclusion by evolutionary trends of
the combination of short plants producing bigger seeds.
Within this group, the seed usually falls due to its own
weight when the capsules are open (barochory). Nevertheless, seeds deposited on the ground, may occasionally be
transported by ants. This fact has been indicated by Van
der Pijl (1982) for Melampyrum and Veronica, and by Berg
(1954) for Pedicularis sylvatica.
Among the genera of this second group, Cymbalaria, is,
perhaps, the best example of atelechory. Capsules of the
species studied of this genus (C. muralis) have negative
phototropism, and two seeds are always retained in the
capsule, easily reaching the substratum.
It is important to mention that the majority of the
examined genera have light or very small seeds, that
facilitate the existence of a double dispersal mechanism
(diplochory) together, in some cases, with myrmecochory
and anemochory, or any other dispersal mechanism.
Phenetic analysis
In morphological studies of selected taxa ( for example
families, tribes, genera), it is appropriate to try to establish
the phylogenetic relationships among taxa based on the
assignation of plesiomorphic or apomorphic characters. Les
(1989) commented on the possible evolutionary relationships in Ceratophyllum (Ceratophyllaceae) based on 19
achene characters, and Manning and Goldblatt (1991)
made a similar study in Iridaceae using 36 seed characters.
The software used (NTSYS) displays a single tree among
the possible ones (Fig. 5). In the UPGMA phenogram
based on the morphological and anatomical characters of
the fruit and seed (Tables 2 and 3), two major clusters with
about 25 % similarity were obtained (the groups have been
labelled as shown in Fig. 5). The ®rst includes all genera
studied belonging to tribe Antirrhineae (group A), while
the remaining genera studied form the other group
(group B).
Within group A, two subgroups (AI and AII) are
distinguished with 39 % similarity. Subgroup AI includes
only the genus Cymbalaria, while the remaining genera
from tribe Antirrhineae form subgroup AII . In the latter
subgroup two other subgroups are recognized (AIII and
AIV): Anarrhinum and Kickxia form subgroup AIII with
44 % similarity to subgroup AIV formed by Antirrhinum,
Chaenorrhinum, Misopates and Linaria. Within this last
subgroup, Linaria is the least closely related genus (52 %)
probably due to several di€erences such as type of dehiscence, or absence of epicuticular waxes. With respect to the
other three genera, Antirrhinum and Chaenorrhinum are the
most similar (72 %) mainly due to the characters derived
from the study of the seeds. However, Misopates occur in an
intermediate position between the Antirrhinum±Chaenorrhinum set and Linaria, due to the quite di€erent seed
structures, despite the resemblance of their capsules.
In group B, the genus Verbascum and Scrophularia
(subgroup BI) are the most distinct from the remaining
genera (only 29 % similarity), although, fruit and seed
characters display a 72 % similarity, despite belonging to
two di€erent subfamilies (Verbascoideae and Scrophularioideae, respectively). The rest of the genera of group B (BII)
form two other subgroups with only 32 % similarity (BIII
Juan et al.ÐFruits and Seeds of Scrophulariaceae
20
40
60
AI
A
100
AIII
Cymbalaria
Anarrhinum
AIV
Kickxia
Antirrhinum
Chaenorrhinum
Misopates
Linaria
AII
BI
BIII
B
80
333
BII
BIV
Verbascum
Scrophularia
Gratiola
Pedicularis
Bartsia
Odontites
Bellardia
Parentucellia
Digitalis
Sibthorpia
Veronica
Erinus
F I G . 5. UPGMA phenogram of Scrophulariaceae genera clustered on the basis of capsule and seed features.
and BIV). On the one hand, subgroup BIII is formed by
Gratiola and Pedicularis, although both genera are quite
di€erent according to the studied characters (only 40 %
similarity), belonging to the subfamilies Scrophularioideae
and Rhinanthoideae, respectively. On the other hand,
subgroup BIV includes the remaining genera belonging to
the subfamily Rhinanthoideae. Within this group, the
genera Bartsia, Odontites, Bellardia and Parentucellia (all
belonging to the tribe Rhinantheae) form a very distinct
group with more than 50 % similarity; Bartsia and
Odontites are two very close genera according to the characters considered for this analysis (94 % similarity), while
Bellardia and Parentucellia also show a relatively high
percentage similarity (75 %). The other four genera (Digitalis, Sibthorpia, Veronica and Erinus) form a very heterogeneous group, being members of three di€erent tribes.
Digitalis remains isolated from the other three genera by
only a 42 % similarity, despite belonging, with Erinus, to
the tribe Digitaleae. The di€erent sizes of the capsules and
seeds, di€erent kinds of indumentum, and di€erent kinds of
reinforcement of the radial wall of the seed epidermis are
responsible for this separation. Finally, the genera Veronica
and Sibthorpia, belonging to the tribes Veroniceae and
Sibthorpieae respectively, are mainly related by the resemblance of their capsules, although all the seed characters are
considerably di€erent.
This study of similarities between the di€erent genera
considered could help our understanding of evolutionary
trends. However, this kind of study is more dicult to
perform because of the lack of usable information about the
evolutionary lines in some or most of the characters used, or
the appropriate selection of the outgroup. All these aspects
must be supported by other more precise work revising each
group of characters. For the characters investigated, such as
dehiscence type, development of the endosperm or embryo
size, some authors such as Takhtajan (1991) established a
reasonable relationship between primitive ( plesiomorphic)
or advanced (apomorphic) stages. Thus, it is possible that in
the near future enough new information will be available to
enable us to reach a good level of understanding of the
phylogenetic relationships in this and other important plant
families. Meanwhile, the use of characters derived from the
study of fruit and seed constitutes a valuable source of
information at generic or tribal levels.
Based on sequences for three chloroplast genes, Olmstead
et al. (1998) indicated that some tribes such as Calceolarieae, Gratioleae pro parte, etc. are not included in the clade
designated ScrophulariaceaeÐevidence that it is a polyphyletic group in its traditional circumscription. Moreover,
some authors (Young et al., 1997, 1999; Wolfe and
dePamphilis, 1998) include all parasitic Scrophulariaceae
within the Orobanchaceae broadly de®ned. Nevertheless,
Thorne (1992) using morphological and molecular data
extend the traditional concept of Scrophulariaceae, including the Orobanchaceae as subfamily Orobanchoideae.
Similarly, Takhtajan (1997) considered this subfamily to
be included in Scrophulariaceae as an advanced group with
parasitic tendencies. The present analysis highlights the
high heterogeneity existing within the Scrophulariaceae,
which may be observed at the subfamily or tribe level. Only
genera belonging to the tribe Antirrhineae are clearly
separated (only by 25 %) from the rest of the genera studied
in the family. These results have aspects in common with
cladograms proposed by Olmstead and Reeves (1995) and
Young et al. (1999), based on molecular data. In agreement
with these authors, Scrophularia and Verbascum are closely
related genera. However, in the present paper, genera such
as Digitalis or Veronica are clearly di€erent from Antirrhinum, although the authors previously cited included
Digitalis and Veronica in Antirrhinaceae with other genera
334
Juan et al.ÐFruits and Seeds of Scrophulariaceae
such as Antirrhinum. Nevertheless, the heterogeneity shown
by morphological and anatomical data of fruits and seeds
could be related to the probable polyphyly of the
Scrophulariaceae.
L I T E R AT U R E C I T E D
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336
Juan et al.ÐFruits and Seeds of Scrophulariaceae
APPENDIX 1
Key to Genera from southwest Spain based on seed features
1.
1.
2.
2.
3.
3.
4.
4.
5.
5.
6.
6.
7.
7.
8.
8.
9.
9.
10.
10.
11.
11.
12.
12.
13.
13.
14.
14.
15.
15.
16.
16.
17.
17.
18.
18.
19.
19.
20.
20.
21.
21.
22.
22.
23.
23.
24.
24.
25.
25.
Capsule with unequal loculi. Dorsi ventral symmetry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
Capsule with subequal loculi. Bilateral or radial symmetry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
Capsule dehiscing by 2 irregularly-toothed pores in the abaxial loculus and 1 in the adaxial. Septum sinuate . . . 3
Capsule dehiscing by 1 pore in each loculus or not any. Septum not sinuate. . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Surface with polygonal cells. Smooth hairs with uniform distribution . . . . . . . . . . . . . . . . . . . . . . . . Antirrhinum
Surface with irregular cells of sinuous margin. Verrucate hairs with uniform distribution or at the apex. . . Misopates
Capsule with apiculate abaxial loculi. Dehiscence loculicidal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pedicularis
Capsule without apiculate abaxial loculi. Dehiscence septicidal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Capsule with glandular and eglandular hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chaenorrhinum
Capsule glabrous or with glandular hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Linaria
Capsule with exclusive septicidal dehiscence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Capsule with di€erent dehiscence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Capsule glabrous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Scrophularia
Capsule tomentose, pubescent or puberulent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Capsule with branched hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Verbascum
Capsule no hair or unbranched . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Capsule ovoid, conical or ellipsoid. Glandular hairs with unicellular obovoid head . . . . . . . . . . . . . . . . . . Digitalis
Capsule globose or subglobose. Glandular hairs with truncate depressed head with at least two cells . . . Verbascum
Capsule with exclusive loculicidal dehiscence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Capsule with di€erent dehiscence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Capsule with unicellular eglandular hairs with enlarged base. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
Capsule without unicellular eglandular hairs with enlarged base . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
Capsule 44.0 mm in width, glandular hairs with elliptical head . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bellardia
Capsule 54.0 mm in width, without glandular hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Capsule with acute apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parentucellia
Capsule with truncate or slightly emarginate apex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Capsule 57.5 mm in length. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Odontites
Capsule 57.5 mm in length. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Surface with rugate cuticle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Odontites
Surface with smooth cuticle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bartsia
Capsule width 42.5 mm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Veronica
Capsule width 4 2.5 mm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Capsule length 4 2.0 mm, with truncate or slightly emarginate apex and eglandular hairs. . . . . . . . . . . .Sibthorpia
Capsule length 42.0 mm, with acute and glabrous apex. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parentucellia
Dehiscence septicidal and loculicidal. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Dehiscence foraminal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
Capsule pubescent, villose or puberulent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
Capsule glabrous or glabrescent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Capsule compressed, 56 mm in length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Veronica
Capsule not compressed, 46 mm in length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Digitalis
Capsule length 54.5 mm, with scarcely any hairs. Pericarp 5100 mm thick . . . . . . . . . . . . . . . . . . . . . . . . Erinus
Capsule length 54.5 mm, glabrous. Pericarp 4100 mm thick . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gratiola
Capsule with glandular and eglandular hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Capsule glabrous or with only glandular hairs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
Capsule with less than 30 seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kickxia
Capsule with more than 30 seeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chaenorrhinum
Each loculus dehiscing by solitary, elongate pore opening by one valve with parallel-sided . . . . . . . . . . Anarrhinum
Each loculus dehiscing by solitary pore, opening by several valves without parallel-sided . . . . . . . . . . . . . . . . . . 25
Capsule with truncate apex. Pores with irregular valves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cymbalaria
Capsule with rounded or slightly emarginate apex. Pores with regular valves. . . . . . . . . . . . . . . . . . . . . . . . Linaria
Juan et al.ÐFruits and Seeds of Scrophulariaceae
337
APPENDIX 2
Key to Genera from southwest Spain based seed features
1.
1.
2.
2.
3.
3.
4.
4.
5.
5.
6.
6.
7.
7.
8.
8.
9.
9.
10.
10.
11.
11.
12.
12.
13.
13.
14.
14.
15.
15.
16.
16.
17.
17.
18.
18.
19.
19.
20.
20.
21.
21.
22.
22.
23.
23.
24.
24.
25.
25.
Seeds discoid, more or less winged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Linaria
Seeds not discoid, not winged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
Seeds with alveoli arranged in longitudinal rows. Endosperm ruminate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Seeds without alveoli arranged in longitudinal rows. Endosperm not ruminate . . . . . . . . . . . . . . . . . . . . . . . . . 4
Endothelium reduced to a dense layer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Scrophularia
Endothelium reduced to a ®lamentous layer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Verbascum
Seeds with a white lateral and spongy appendix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pedicularis
Seeds without a lateral appendix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Cells of seed epidermis with membranous outer tangential walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
Cells of seed epidermis without membranous outer tangential walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
Seed-coat with longitudinal ridges or wings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Seed-coat without longitudinal ridges or wings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Seeds length 51.0 mm. Inner tangential walls granulate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bellardia
Seeds length 41.0 mm. Inner tangential walls reticulate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bartsia, Odontites
Seed-coat reticulate-alveolate or irregularly cristate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kickxia
Seed-coat reticulate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Seeds strongly depressed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Veronica
Seeds not depressed. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Seeds dark brown to black in color. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Seeds brown to yellowish in color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
Seeds ellipsoid, with a broad cavity in the ventral face. Subterminal funicular attachment. Radial walls not
perforate. Little embryo, 51/3 in relation to endosperm length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Sibthorpia
Seeds prismatic or cylindric, without a broad cavity in the ventral face. Terminal funicular attachment. Radial
walls perforate. Embryo aproximaly 1/2 in relation to endosperm length . . . . . . . . . . . . . . . . . . . . . . . . . Digitalis
Seeds with a furrow in the ventral face . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Seeds without a furrow in the ventral face . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Seeds 41 mm in length. Alveolate radial walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Digitalis
Seeds 51 mm in length. Reticulate radial walls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Erinus
Seeds with faint longitudinal bulges superimposed by a reticulate pattern . . . . . . . . . . . . . . . . . . . . . . Parentucellia
Seeds without longitudinal bulges. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Seed-coat with reticle formed by elongate cells. Embryo aproximaly 1/2 in relation to endosperm . . . . . Parentucellia
Seed-coat with reticle formed by square cells. Endosperm occupied by embryo nearly as a whole . . . . . . . . Gratiola
Seeds yellowish to brown in color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Veronica
Seeds black to black-brown in color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Seeds cyathiform. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Veronica
Seeds not cyathiform . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Seeds medusiform, with an encircling ridge in the ventral face . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Misopates
Seeds di€erent in shape, without an encircling ridge in the ventral face . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Seeds trigonous, tetrahedral or reniform. With or without transverse ridges . . . . . . . . . . . . . . . . . . . . . . . . Linaria
Seeds globoses or ellipsoid. Without transverse ridges. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
Seed-coat reticulate alveolate. Without epicuticular waxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kickxia
Seed-coat cristate or tuberculate. With or without epicuticular waxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Seed-coat with tubercles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
Seed-coat with ridges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Tubercles broad based, obtuse, with globose cells and without intertubercular space . . . . . . . . . . . . . . . . . Kickxia
Tubercles conical, acute, with concave cells and with intertubercular space . . . . . . . . . . . . . . . . . . . . . Anarrhinum
Seeds with longitudinal ridges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
Seeds with irregular ridges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Ridges anastomosed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Antirrhinum
Ridges not anastomosed, sometimes discrete . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chaenorrhinum
Ridges with cells more large than interstice cells. Epicuticular waxes present. . . . . . . . . . . . . . . . . . . . Cymbalaria
Ridges cells with similar size to intersticial cells similar in size. Epicuticular waxes absent . . . . . . . . . . . . . Kickxia
338
Juan et al.ÐFruits and Seeds of Scrophulariaceae
APPENDIX 3
Part of the material examined in the present study was previously the subject of more detailed anatomical and
morphological studies of the genera. Thus, after mentioning determined genera, we include a reference to the complete lists
of species, localities, and herbarium codes of the studied material (mainly from southwest Spain). For the rest of examined
material we list all collecting data:
Anarrhinum: A. bellidifolium, A. laxi¯orum, see Juan et al. (1996d).
Antirrhinum: A. australe, A. barrelieri, A. graniticum subsp. boissieri, A. graniticum subsp. boissieri, A. majus subsp.
majus, A. majus subsp. cirrhigerum, A. majus subsp. tortuosum, see Juan, Pastor and FernaÂndez (1996a).
Bartsia: B. aspera. SPAIN. CAÂDIZ. Los Barrios, cuevas La Bruja, 17.9.1972, Allen (SEV 12730), PORTUGAL. Coimbra,
11.8.1977, Malato-BeÂliz & Guerra (SEV 42575).
Bellardia: B. trixago. SPAIN. CAÂDIZ, Bornos, 7.5.1992, Arista & Talavera (SEV 135217). Between Jerez de la Frontera
and Alcala de los Gazules, 15.6.1992, FernaÂndez & Juan (SEV 135218). COÂRDOBA. Alcaracejos, 6.5.1992, Juan
(SEV 135219). Between El Vacar and Obejo, 9.6.1992, Juan and Pastor (SEV 135220). HUELVA. Between La Granada
de RõÂ o Tinto & CampofrõÂ o, 31.5.1992, Santa-BaÂrbara (SEV 135221).
Chaenorrhinum: C. macropodum subsp. degenii, C. rubrifolium subsp. rubrifolium, C. villosum subsp. villosum, C. villosum
subsp. granatensis, see Juan et al. (1997b).
Cymbalaria: C. muralis. SPAIN. HUELVA. Punta UmbrõÂ a, 17.4.1992, Juan & LoÂpez (SEV 135183). RõÂ o Tinto, 24.3.1992,
Santa-BaÂrbara (SEV 135184). Fuenteheridos, 18.8.1993, Juan & LoÂpez (SEV 135185). SEVILLA. Sevilla, 11.4.1993,
Arista (SEV 135186).
Digitalis: D. obscura subsp. obscura, D. purpurea subsp. purpurea, D. purpurea subsp. bocquetii, D. purpurea subsp.
heywoodii, D. purpurea subsp. mariana, D. thapsi, see Juan et al. (1998a).
Erinus: E. alpinus. SPAIN. CAÂDIZ. Grazalema, San CristoÂbal, 28.9.1979. DõÂez, Romero & ValdeÂs (SEV 74784). Idem, Pico
del Pinar, 20.5.1981, Gallego, GarcõÂa & Silvestre (SEV 125653). Idem, Puerto de las Palomas, 27.5.1992, Juan & Pastor
(SEV 135262). JAEÂN. Sierra de Cazorla, 25.5.1993, Arista (SEV 135263).
Gratiola: G. linifolia. SPAIN. HUELVA. Almonte, DonÄana, laguna de Santa Olalla, 16.5.1981, Talavera & ValdeÂs (SEV
96652). Rõ o Tinto, 5.6.1992, Juan, Pastor & Santa-BaÂrbara. G. ocinalis. SPAIN. GERONA. Cantallops, 6.8.1990,
Molero y Rovira (SEV 94401). FRANCE. Ried Saint-Hyppolyte, 17.8.1979, Schneider (SEV 80018).
Kickxia: K. cirrhosa, K. elatine, K. lanigera var. lanigera, K. lanigera var. dealbata, K. spuria subsp. integrifolia, see Juan
et al. (1998c).
Linaria: L. aeruginea, L. amethystea subsp. amethystea, L. amethystea subsp. multipunctata, L. anticaria, L. caesia, L. hirta,
L. huteri, L. incarnata, L. polygalifolia subsp. lamarckii, L. latifolia, L. micrantha, L. munbyana var. munbyana,
L. munbyana var. pygmaea, L. oblongifolia subsp. haenseleri, L. pedunculata, L. platycalyx, L. saxatilis, L. spartea var.
spartea, L. spartea var. praecox, L. tartessiana, L. triphylla, L. tristis, L. tursica, L. viscosa, see Juan, FernaÂndez and
Pastor (1999a), Juan et al. (1999c).
Misopates: M. orontium var. orontium, M. orontium var. grandi¯orum, see Juan et al. (1995).
Odontites: O. foliosa, O. longi¯ora, O. tenuifolia, see Juan et al. (1996b).
Parentucellia: P. latifolia, P. viscosa, see Juan et al. (1998b).
Pedicularis: P. sylvatica subsp. lusitanica, see Juan et al. (1996c).
Scrophularia: S. canina subsp. canina, S. crithmilfolia, S. frutescens, S. laevigata, S. lyrata, S. oxyrrhyncha, S. peregrina,
S. sambucifolia subsp. sambucifolia, S. sambucifolia, subsp. mellifera, S. scorodonia, see Juan et al. (1999d).
Sibthorpia: S. europaea, see Juan et al. (1999b).
Verbascum: V. barnadesii, V. dentifolium, V. erosum, V. giganteum subsp. giganteum, V. giganteum subsp. martinezii,
V. masguindali, V. pulverulentum, V. rotundifolium subsp. haenseleri, V. simplex, V. virgatum, see Juan et al. (1997c).
Veronica: V. agrestis, V. anagallis-aquatica, V. anagalloides, V. arvensis, V. cymbalaria, V. hederifolia subsp. hederifolia,
V. hederifolia subsp. triloba, V. peregrina, V. persica, V. polita, V. praecox, V. scutellata, V. triphyllos, see Juan et al.
(1994, 1997a)