Botanical Journal of the Linnean Society, 2002, 139, 87–98. With 12 figures
Gametophyte morphology and gametangial ontogeny
of Asplenium foreziense and related taxa
(Aspleniaceae: Pteridophyta)
ALBERTO HERRERO*, CARMEN PRADA and SANTIAGO PAJARÓN
Departamento de Biología Vegetal I, Facultad de Biología, Universidad Complutense, E-28040
Madrid, Spain
Received April 2001; accepted for publication January 2002
Gametophytes of Asplenium foreziense and related taxa have been studied by culture of spores on mineral agar and
soil. Those of A. obovatum ssp. obovatum var. protobillotii and var. deltoideum, ssp. numidicum, and of A. macedonicum are described for the first time. Gametophyte development follows the Adiantum type in the A. obovatum
group, and the Aspidium type in A. fontanum. Both types of development have been found in A. foreziense, depending on the sporophytic sample. The taxa with hairy gametophytes show significant differences in hair density. As
in most of the homosporous ferns, antheridia are formed first and in a high proportion of gametophytes in the A.
obovatum group and in A. fontanum, except for one sample; most of these male gametophytes become bisexual. In
A. foreziense and A. macedonicum archegonia are formed first or at the same time as antheridia, but the proportion of female gametophytes is higher than in the other taxa; some of the gametophytes become bisexual, most of
them differentiated from the female ones. © 2002 The Linnean Society of London, Botanical Journal of the Linnean
Society, 2002, 139, 87–98.
ADDITIONAL KEYWORDS: morphology – reproductive biology – sex expression – spore germination –
taxonomy.
INTRODUCTION
Asplenium foreziense Legrand ex Hérib. is an allotetraploid derived by polyploidization after hybridization of two diploids, A. obovatum Viv. ssp. obovatum
and A. fontanum (L) Bernh. (Sleep, 1967, 1983). For
A. fontanum, two subspecies have been proposed
(Reichstein & Schneller, 1982), ssp. fontanum from
Europe and North Africa, and ssp. pseudofontanum
(Kossinsky) Reichst. & Schneller from the Himalaya.
The sporophytic characters are very similar in both
subspecies, the disjunct area being the main reason
for their taxonomic differentiation. The complex A.
obovatum, of Mediterranean, Atlantic and Macaronesian distribution, was studied by Demiriz, Viane &
Reichstein (1990), who recognized a diploid subspecies, ssp. obovatum with three varieties (obovatum,
*Corresponding author. Current address: Real Jardín
Botánico, Plaza de Murillo 2, E-28014 Madrid, Spain. E-mail:
[email protected]
protobillotii Demiriz, Viane & Reichst. and deltoideum
Demiriz, Viane & Reichst.), and a tetraploid one,
ssp. lanceolatum (Fiori) P. Silva (= A. billotii F. W.
Schultz). In this group of taxa, differences in the
morphology of the sporophytes with regard to frond
outline and shape of foliar segments and teeth are
evident. A different taxon from North Africa, tetraploid and also related to this group, is treated by some
authors (Battandier & Trabut, 1902; Maire, 1952;
Salvo et al., 1992) as A. obovatum ssp. numidicum
(Trab.) Salvo & Cabezudo. Other authors treated
(Becherer, 1935) or suggested (Rumsey & Vogel, 1996)
A. obovatum ssp. numidicum as synonymous with
A. foreziense. A. foreziense is present in scattered
populations in the western Mediterranean region.
Based on subtle sporophytic differences of Macedonian populations, A. macedonicum was described as a
different species by Kümmerle (1916) but its validity
is now rejected (Viane, Jermy & Lovis, 1993). Although
systematic studies on ferns are mainly based on
sporophytes, gametophytic characters have been used
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in some cases and can contribute to a better understanding of fern evolution (Stokey, 1951; Miller, 1968;
Nayar & Kaur, 1971; Atkinson, 1973; Windham &
Haufler, 1986). The gametophyte generation of this
Asplenium group has been studied (Momose, 1960;
Henriet, 1970; Henriet & Moens, 1976; Henriet,
Auquière & Moens, 1976; Prada et al., 1996). Most of
these studies have focused on gametophyte development and morphology; only a few data on reproductive
biology were obtained, even the morphology of some of
the recognized taxa was not known.
Our purpose has been to complete the study of
gametophyte morphology of this group of taxa and
evaluate the taxonomic implications of morphological
characters and to study gametangial ontogeny and
sexual expression under laboratory conditions.
MATERIAL AND METHODS
Spores for gametophyte cultures were obtained from
the collections indicated in the Appendix. Each spore
sample for cultures was taken from a single sporophyte. Voucher specimens are deposited in the MACB
herbarium (Herbarium of the Facultad de Biología de
la Universidad Complutense de Madrid).
Spores were sown on mineral agar (Dyer, 1979) in
6 cm diameter Petri dishes for the study of germination rate, early stages of gametophyte development,
and as a source of young presexual prothalli. Cultures
were sampled every two days during the first month
after sowing. Each sample was also sown on sieved soil
(a 3 : 1 mixture of compost and sand), sterilized in a
stove at 120 °C for 2 h to prevent germination of spores
from the natural spore bank, and rehydrated in the
Petri dishes in order to complete the morphological
study and obtain mature prothalli. Sowings of each
sample were replicated twice on both agar and soil
media to produce enough gametophytes for sampling.
The dishes were kept in a growth chamber at
20° ± 2 °C, under 12 h of illumination with white fluorescent tubes (28 mE m–2 s–1)/12 h of dark. Soil cultures
were watered once a week.
Random samples of approximately 50 gametophytes
of each culture on soil were taken weekly after reaching the bidimensional stage, stained with chloral
hydrate acetocarmine (Edwards & Miller, 1972),
mounted in water, and observed under a light microscope to complete the morphological study of prothalli
in their different stages of development. In hairy
prothalli, length and density of marginal hairs were
measured on mature female or bisexual gametophytes
(4–5 mm wide). Length was calculated, using a light
microscope, by measuring three hairs in each of ten
different gametophytes (30 measurements) from each
culture. Density (number of hairs mm-1) was obtained,
using an image-analysing computer (Microm,
Barcelona) by examining 30 gametophytes randomly
sampled from each culture. Mean and standard
deviation were calculated for each parameter. A
Kruskal–Wallis test was performed to test for differences in each parameter.
To study the ontogenetic sequence of gametangia
and sex expression, 50 presexual prothalli were transplanted from agar cultures to Petri dishes with soil
prepared as indicated above. Prothalli were planted
in a regular pattern to achieve a homogeneous density
(c. 1 prothallus 0.50 cm-2). Individual gametophytes
were examined weekly to detect initial sex expression and progression along the period of observation;
these observations were made until the cultures
stabilized and percentages of each sexual type did not
change. Samples used in this study were: BET19 and
BUJ1 for A. fontanum ssp. fontanum, TR7400 for A.
fontanum ssp. pseudofontanum, BEA20 and VAR7
for A. obovatum var. obovatum, MIE27 and MIE41 for
A. obovatum var. protobillotii, AH84F and NAV8 for
A. obovatum ssp. lanceolatum, MGC 28503 for A.
obovatum ssp. numidicum, AH115F and BUF10 for
A. foreziense, and J1 and J2 for A. macedonicum.
A. obovatum var. deltoideum could not be included
because there were insufficient gametophytes from the
parental sample.
RESULTS
SPORE
GERMINATION, DEVELOPMENT AND
MORPHOLOGY OF GAMETOPHYTES
Spore germination started 5–17 days after sowing,
depending on the age of the sample, i.e. the time
between collection and sowing. Spores from recently
collected sporophytes required, in general, less time to
germinate and reached higher percentages of germination than the ones obtained from sporophytes collected earlier (Table 1). Spore germination is of the
Vittaria type (Nayar & Kaur, 1968); the spore cell
grows and emerges from the lesure. The first division
parallel to the equatorial plane of the spore separates
a small hemispherical cell. The first rhizoid usually
emerges from the basal cell. Successive divisions
produce a germ filament with 1–6 cells.
The bidimensional phase started between 15 and
20 days after germination, following the Adiantum
type of development (Nayar & Kaur, 1969, 1971) in all
taxa except in A. fontanum and in most of the samples
of A. foreziense (AH115F, BUF10 and FRA2). This type
of development is characterized by the formation of
an oblique wall in the terminal cell of the filament;
a cuneiform cell is differentiated, from which, after
several divisions, a meristem is formed. Later a
symmetrical, cordate and naked plate is produced
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GAMETOPHYTES OF ASPLENIUM FOREZIENSE AND RELATED TAXA
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Table 1. Spore age (months), time to germination (days), percentage of germination (%) and time to maximum germination rate (days)
Taxon
sample
Spore
age
A. fontanum ssp. fontanum
BAI14
BET19
BUJ1
GOR1
5
7
7
7
6
9
6
8
90
90
98
94
64
45
37
64
A. fontanum ssp. pseudofontanum
TR7400
TR7402
40
40
15
17
16
59
86
86
A. obovatum var. obovatum
BEA20
BON20
VAR7
2
2
8
7
7
5
100
100
100
17
17
17
A. obovatum var. deltoideum
Ras-1022
28
10
81
52
A. obovatum var. protobillotii
MIE27
MIE41
Ras-610
7
7
83
6
7
9
100
100
56
24
29
86
A. obovatum ssp. lanceolatum
AH84F
ITA12
NAV8
TUY6
9
17
11
9
5
6
6
7
94
100
100
96
64
15
15
23
A. obovatum ssp. numidicum
MGC 28503
40
7
84
55
A. foreziense
AH115F
BUF10
CAB9
FRA2
9
13
2
18
5
6
6
7
100
100
100
96
52
15
12
64
A. macedonicum
J1
J2
78
174
13
13
74
30
46
46
(Figs 1A–G, 2), which is very similar in all the taxa of
this group.
In both subspecies of A. fontanum and in most of the
samples of A. foreziense gametophyte development
follows the Aspidium type (Nayar & Kaur, 1969, 1971),
in which there is an early formation of a hair in the
young gametophyte (Figs 1E–G, 3, 4); new hairs are
formed as the gametophyte grows. Mature gametophytes bear hairs on the surface and margins; most of
the hairs are unicellular, cylindrical, and of the papillose type (Stokey, 1951), sometimes wider at the base.
Bicellular hairs are common in A. fontanum ssp.
fontanum (Fig. 3) and occasionally tricellular ones
(sample BAI14). In the hairy samples of A. foreziense
unicellular and bicellular hairs are also produced
(Fig. 4). A. fontanum ssp. pseudofontanum only has
unicellular hairs. The apex of the hairs on fresh gametophytes always shows an exudate that is of unknown
function and composition (Fig. 5).
Time to
germination
Percentage
germination
Time to max.
germinatation rate
As in A. foreziense, hairy and naked gametophytes
were found depending on the sporophytic individual,
we repeated new sowings using six additional individuals from population CAB and nine from population FRA. The gametophytes obtained from CAB were
hairy in five samples and naked in one; in contrast, all
gametophytes from FRA were hairy.
The taxa with hairy gametophytes frequently show
the lateral wings with an irregular outline due to the
proliferation of cells in rows of decreasing size that
normally end in a unicellular or bicellular hair (Fig. 6).
In mature prothalli some of the hairs become empty
and detach from their base leaving a scar in the supporting cell (Fig. 7). A similar situation was reported
for A. trichomanes ssp. trichomanes (Herrero et al.,
1993), but in this case the gametophytes do not become
naked.
Hairy gametophytes in this group of taxa have different density of hairs; in the margin of the prothalli
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A. HERRERO ET AL.
notch (Figs 10, 11). When bicellular hairs are present,
they are formed in higher proportion on female and
bisexual gametophytes than on the male ones
(Table 2).
GAMETANGIAL
ONTOGENY AND SEX EXPRESSION
Gametophytes started to show sex expression between
61 and 82 days after sowing (Fig. 12). Male gametangia were produced before or at the same time as the
female ones. In A. fontanum and A. obovatum (except
in sample VAR7 of var. obovatum), male gametophytes
were differentiated in a high proportion ranging from
74 to 100%; depending on the sample, between 46 and
88% of male gametophytes became bisexual. In six
samples of these taxa a small proportion of female
gametophytes was formed; half remained as females
but the other half became bisexual so that by the end
of the period of observation three types of gametophyte
coexisted (Table 4).
In A. foreziense and A. macedonicum the progression
of sex expression differed as female prothalli were
produced in higher proportions than the male ones;
these proportions ranged from 32 to 94%. In sample
J1 of A. macedonicum antheridia and archegonia were
formed simultaneously in 56% of the prothalli. With
the exception of sample J1, bisexual gametophytes
were produced in lower proportions than in A.
fontanum and A. obovatum, and they arose mainly
from the female ones (Table 4). At the end of the observation period the three sex expressions coexisted.
Similar behaviour was observed in sample VAR7 of A.
obovatum var. obovatum (Fig. 12; Table 4).
DISCUSSION
Figure 1. Early stages of prothallial development: A-G,
Adiantum type; A-G’, Aspidium type. Scale bar = 0.1 mm.
density is lower in A. foreziense (Figs 3, 4), with a
mean value of 3.49 hairs mm-1, than in A. fontanum
ssp. fontanum and ssp. pseudofontanum that had
mean values of 11.01 and 9.12 hairs mm-1, respectively. We also found a higher frequency of bicellular
hairs in A. foreziense (Table 2). Length of marginal
hairs is different among taxa, but this is a variable
character. Asplenium fontanum tends to have shorter
hairs than A. foreziense (Table 3).
Mature prothalli in all taxa of this group show a
sexual dimorphism (Fig. 8). Male gametophytes are
spatulate and usually lack the apical notch; they are
smaller and more irregular in shape than the female
and bisexual ones (Fig. 9). The last two sexual types
are very similar, cordate and with an evident apical
The viability of spores in pteridophytes is very
variable depending on the taxa and storage conditions. Lloyd & Klekowski (1970) indicated a mean of
2.8 years for the species of ferns with nongreen spores
kept under ordinary storage conditions. It is also a
common fact that in old spores, percentages of germination decrease and gametophytes obtained from
them can show abnormalities in their growth pattern
(Raghavan, 1989). The viability of spores in the group
of taxa studied agrees with the behaviour expected for
this kind of fern. Some of the samples exceeded the
average of life span indicated as shown above; in the
case of sample Ras-610 of A. obovatum var. protobillotii and sample J2 of A. macedonicum, more than 6
and 14 years old, respectively. Percentages of germination in these samples were lower than in most of the
younger ones, but we have not observed abnormalities
in the gametophytes obtained.
Gametophytes in this group of taxa show two main
morphologies, naked in A. obovatum and hairy in A.
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GAMETOPHYTES OF ASPLENIUM FOREZIENSE AND RELATED TAXA
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91
3
4
5
6
7
Figures 2–7. Detail of margin of mature gametophytes. Fig. 2. Asplenium obovatum ssp. obovatum var. obovatum. Scale
bar = 50 mm. Fig. 3. A. fontanum ssp. fontanum. Scale bar = 50 mm. Fig. 4. A. foreziense. Scale bar = 50 mm. Fig. 5. Exudate
of marginal hairs. Scale bar = 10 mm. Fig. 6. Proliferation of cells in margin of prothallus of A. fontanum ssp. fontanum.
Scale bar = 50 mm. Fig. 7. Empty and detached marginal hair of A. fontanum ssp. fontanum. Scale bar = 20 mm.
fontanum. Only in A. foreziense have both types of
gametophytes been found depending on the sporophyte from which spores were taken. The presence of
hairs in gametophytes is usually a fixed character; we
only know the case of A. trichomanes ssp. quadri-
valens for which hairy and naked gametophytes were
described, and which were produced by the same
parent sporophyte (Herrero et al., 1993). The sample
of A. foreziense studied by Henriet & Moens (1976) was
of the hairy type and they interpreted this character
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A. HERRERO ET AL.
Table 2. Percentage of prothalli with bicellular hairs in the different sexual types
of each sample
Percentage of prothalli with
bicellular hairs
Taxon
sample
A. fontanum ssp. fontanum
BAI14
BET19
BUJ1
GOR1
A. fontanum ssp. pseudofontanum
A. foreziense
Males
Females
Bisexuals
0
0
0
0
71
0
23
8
31
0
11
18
TR7400
TR7402
0
0
0
0
0
0
BUF10
AH115F
FRA2
23
0
10
31
87
84
80
50
67
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GAMETOPHYTES OF ASPLENIUM FOREZIENSE AND RELATED TAXA
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Figures 8–11. Fig. 8. Culture with mature prothalli of sample AH84F of A. obovatum ssp. lanceolatum: () male, (➞)
female, () bisexual. Figs 9–11, silhouettes of mature prothalli of the same sample: Fig. 9, male. Fig. 10, female. Fig. 11,
bisexual. Scale bar = 1 mm.
Table 3. Means and standard deviations of density (number of hairs mm-1) and length (mm) of marginal hairs for each
sample. Test of significance refer to Kruskal–Wallis test. N = 30
A. fontanum ssp. fontanum
BAI14
BET19
BUJ1
GOR1
A. fontanum ssp.
pseudofontanum
A. foreziense
TR7400
BUF10
AH15F
TR7402
Density
mean
SD
12.14
2.04
10.87
1.5
10.54
1.48
10.48
1.22
9.02
1.74
9.23
1.15
4.48
0.6
1.74
0.55
Length
mean
SD
35.33
4.58
36.9
4.18
46.26
5.57
35.06
3.65
37.33
2.59
38.4
4.21
47.96
5.42
69.93
6.37
FRA2
4.26***
0.75
40.73
3.21
***P < 0.001.
Table 4. Percentage of different sex expressions reached at the end of the period of observation. For bisexuals it is indicated whether they developed from males, from females, or if antheridia and archegonia were formed simultaneously
Bisexuals
Taxon
sample
Males
Females
simulataneous
from male
from female
A. fontanum ssp. fontanum
BET19
BUJ1
2
–
10
6
–
–
88
88
–
6
A. fontanum ssp. pseudofontanum
TR7400
12
–
–
84
4
A. obovatum var. obovatum
BEA20
VAR7
32
18
–
40
–
–
68
16
–
26
A. obovatum var. protobillotii
MIE27
MIE41
34
54
–
–
–
–
66
46
–
–
A. obovatum ssp. lanceolatum
AH84F
NAV8
46
34
4
–
–
–
50
50
–
16
A. obovatum ssp. numidicum
MGC 28503
48
–
22
26
4
A. foreziense
AH115F
BUF10
8
10
82
68
–
–
8
22
2
–
A. macedonicum
J1
J2
2
4
6
58
56
–
10
2
26
36
as inherited from its parent A. fontanum. From our
results, it seems that the most frequent morphology
in this taxon is the hairy one, as in its parent A.
fontanum, but with a lower density of hairs. However,
some plants can show the morphology of the other
parent, A. obovatum ssp. obovatum.
Gametophyte characters in these taxa are of
taxonomic value. The information provided by the
gametophytes support the taxonomic scheme accepted
at present. The A. obovatum group is very homogeneous with regard to gametophyte morphology, and
all the taxa discussed as belonging to this group
coincide in their gametophyte characters. The same is
true for A. fontanum ssp. fontanum and ssp. pseudofontanum, where only the subtle difference of lacking
bicellular hairs in the samples studied of the latter
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A. HERRERO ET AL.
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
0%
61
68
75
82
89
106
113
61
68
75
82
89
106
113
120
127
134
141
148
155
61
68
75
82
89
106
113
120
127
134
141
148
155
100%
80%
60%
40%
20%
0%
120
127
134
141
148
155
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
61
68
75
82
89
106
113
120
127
134
141
148
155
Figure 12. Bar diagrams showing sexual expression percentages in each sample. Values of X-axis indicate days from
sowing. ( ) steriles, () females, () males, ( )bisexuals.
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GAMETOPHYTES OF ASPLENIUM FOREZIENSE AND RELATED TAXA
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
95
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
61
68
75
82
89
106
113
120
127
134
141
148
61
68
75
82
89
106
113
120
127
134
141
148
155
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
61
68
75
82
89
106
113
120
127
134
141
148
155
100%
80%
60%
40%
20%
0%
Figure 12. Continued.
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A. HERRERO ET AL.
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
100%
100%
80%
80%
60%
60%
40%
40%
20%
20%
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
61
68
75
82
89
106
113
120
127
134
141
148
155
0%
61
68
75
82
89
106
113
120
127
134
141
148
155
Figure 12. Continued.
taxon is noted. The samples of A. macedonicum
studied were of the naked type, which is not the most
common type in A. foreziense; however, as we found
both gametophyte morphologies in individuals from
the same population of A. foreziense, nothing can be
concluded as to the identity of these taxa, particularly
if their similar behaviour in the sexual expression
is taken into account. In addition, a morphological
(Herrero, 1998) and isozyme electrophoretic (Herrero,
Pajarón & Prada, 2001) study of sporophytes of this
group, demonstrated the identity of both taxa, as
well as the correct inclusion of A. obovatum ssp.
numidicum in the A. obovatum group instead of being
related to A. foreziense.
Regarding the ontogenetic sequence of gametangia,
A. fontanum and A. obovatum are characterized by a
high proportion of male gametophytes which become
bisexual; this is the most general situation for homo-
sporous ferns (Atkinson & Stokey, 1964). Following
Klekowski (1969), this sequence would favour intragametophytic selfing whereas in A. foreziense and
sample VAR7 of A. obovatum var. obovatum the presence of a high proportion of female gametophytes
would favour intergametophytic crossing. Deductions
on mating systems based on ontogenetic sequences
of gametangia are not possible in this case, despite
evident higher or lower probability for any of the
systems depending on the sexual composition of the
gametophyte progeny.
Fern mating systems are complex and can vary
among species and among populations within species
(Soltis & Soltis, 1987). As the results in this study
show, not all samples of the same taxon have the same
sexual behaviour. This can have an evident influence
on the mating system, together with other varied
external factors which are not difficult to understand
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 87–98
GAMETOPHYTES OF ASPLENIUM FOREZIENSE AND RELATED TAXA
and which make these plants extremely plastic in
their ability for reproduction.
ACKNOWLEDGEMENTS
The authors wish to thank Helga Rasbach, Ronnie
Viane and Johannes C. Vogel for providing plant material of A. obovatum var. deltoideum, A. fontanum ssp.
pseudofontanum and A. macedonicum, repectively.
We would also like to thank an anonymous reviewer
for helpful comments and suggestions. This work was
supported by project grant PB94-0317 from the Dirección General de Ciencia y Tecnología (D.G.C.Y.T), and
by a fellowship to A. Herrero from the Ministerio de
Educación y Ciencia (Spain).
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98
A. HERRERO ET AL.
APPENDIX
ASPLENIUM
FONTANUM
ASPLENIUM
(L.) BERNH.
SSP. FONTANUM
BAI14: France, Pyrénées-orientales, Prats-de-Mollo,
défilé de la Baillanouse, 31TDG69, slope on slate rock,
A. Herrero, S. Pajarón, E. Pangua & C. Prada, 18.ix.
1994.
BET19: Spain, Cuenca, Beteta, fuente de los Tilos,
30TWK78, c. 1100 m, crevices on limestone rock, T.
Almaraz, A. Herrero & L. Medina, 29.v. 1995.
BUJ1: Spain, Huesca, Torla, San Nicolás de Bujaruelo,
30TYN33, c. 1300 m, crevices on limestone rock, M. E.
González & A. Herrero, 17.viii. 1994.
GOR1: Spain, Huesca, Fanlo, 31TBH52, c. 2200 m,
crevices on limestone rock, M. E. González & A.
Herrero, 15.viii. 1994.
ASPLENIUM FONTANUM SSP. PSEUDOFONTANUM
(KOSSINSKY) REICHST. & SCHNELLER
TR7400
Swat,
1990.
TR7402
Swat,
(= C.R. Fraser-Jenkins sheet 20): Pakistan,
valley of Kalam, c. 2500 m, rock overhangs,
(= C.R. Fraser-Jenkins sheet 22): Pakistan,
valley of Kalam, 1990.
ASPLENIUM
FOREZIENSE
LEGRAND
EX
HÉRIB.
FRA2: France, Lozère, Ste. Margarite-La Figuère, Les
Cévennes, vallée du Borne, c. 450 m, crevices on
granitic rock, A. Herrero, S. Pajarón, E. Pangua &
C. Prada, 29.viii. 1993.
AH115F: Spain, Almería, Gérgal, sierra de los Filabres,
Calar Alto, 30SWG31, c. 1700 m, crevices on schistous
rock, A. Herrero, E. Pangua & C. Prada, 16.vi. 1994.
BUF10: Spain, Gerona, El Port de la Selva, puig dels
Bufadors, 31TEG28, c. 400 m, crevices on schistous
rock, I. Álvarez Fernández, A. Herrero & N. Yagüe,
4.xii. 1994.
CAB9: Spain, Teruel, Albarracín, sierra de Albarracín,
barranco del Navazo, 30TXK37, c. 1250 m, crevices on
sandstones, G. Aragón, A. Herrero & I. Martínez, 18.v.
1996.
ASPLENIUM
MACEDONICUM
OBOVATUM
VIV.
SSP. OBOVATUM
VAR. OBOVATUM
BEA20: France, Pyrénées-orientales, Port-Vendres, cap
Béar, 31TEH10, c. 50 m, crevices on slate rock, in
sea-cliff, G. Aragón, A. Herrero, I. Martínez & A.
Pujol, 9.xii. 1995.
VAR7: France, Var, Saint Raphaël, Le Dramont, cap
du Dramont, c. 30 m, crevices on siliceous rock, in
sea-cliff, M. Boudrie et al., 27.vii. 1994.
BON20: Spain, Gerona, Cadaqués, cap de Creus, cala
Bona, 31TEG28, c. 50 m, crevices on siliceous rock,
in sea-cliff, G. Aragón, A. Herrero, I. Martínez &
A. Pujol, 9.xii. 1995.
A.
OBOVATUM SSP. OBOVATUM VAR. DELTOIDEUM
DEMIRIZ, VIANE & REICHST.
Ras-1022: France, Finistère, cap Brezellec, H. Rasbach,
K. Rasbach & R. Viane, 21.vi. 1995.
ASPLENIUM
VIV. SSP. OBOVATUM VAR.
DEMIRIZ, VIANE & REICHST.
OBOVATUM
PROTOBILLOTII
MGC 32201: Spain, Cádiz, Algeciras, Miel valley, c. 5 km
W. of Algeciras, c. 110 m alt., H. Rasbach, K. Rasbach
& H.W. Bennert Ras-610, 15.iv. 1988.
MIE27 and MIE41: Spain, Cádiz, Algeciras, valle del
río de la Miel, 30STE79, c. 200 m, on sandstones, A.
Herrero, 14.v. 1995.
ASPLENIUM
OBOVATUM SSP. LANCEOLATUM
(FIORI) P. SILVA
ITA12: Italy, La Spezia, Cinque Terre, monte della
Madonna, c. 150 m, crevices on sandstones artificial
wall, A. Herrero, S. Pajarón, E. Pangua & C. Prada,
23.vii. 1994.
AH84F: Spain, Cádiz, Algeciras, valle del río de la Miel,
30STE79, c. 200 m, on sandstones, A. Herrero, E.
Pangua & C. Prada, 14.vi. 1994.
NAV8: Spain, Toledo, Los Navalucillos, Montes de
Toledo, valle del arroyo del Chorro, 30SUJ57, c.
750 m, crevices on slate rock, G. Aragón, A. Herrero &
I. Martínez, 2.iv. 1995.
TUY6: Spain, Pontevedra, Tuy, crevices on granitic
artificial wall, S. Pajarón & E. Pangua, 18.vi. 1994.
KÜMMERLE
J1: Macedonia, Prilep, 1960–70 (without precise date),
A. Sleep. Fronds detached the 10.viii. 1981 from
cultivated plant.
J2: Macedonia, Prilep, A. Sleep, 20.ix. 1973. Fronds
detached the 10.viii. 1981 from cultivated plant.
ASPLENIUM
OBOVATUM SSP. NUMIDICUM
(TRAB.)
SALVO & CABEZUDO
MCG 28503: Morocco, Tanger, Mediuna, sandstones,
30STE37, B. Cabezudo et al. 277/90, 14.v. 1990.
© 2002 The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 139, 87–98