Aspects of Spore Dispersal in Selaginella

11 Pages·1997·6.5 MB·English

by  Agata Filippini-De Giorgi

American Fern
Journal 87(3):g
Aspects of Spore Dispersal Selaginella
in
memory
Tadeus
Dedicated to the of Prof Dr. Reichstein
.
Agata
Giorgi
Filippini-De
ETHZ,
Geobotanisches
Institut Ziirichbergstr. 38,
CH-8044 Switzerland
Zurich,
Rolf Holderegger^ and Johann Jakob Schneller
Systematische Botanik, Universitat Zurich, Zollikerstr. 107,
Institut
fiir
Assuming
Abstract.—The evolution of heterospory changed the conditions for spore dispersal.
wind the dispersal agent, microspores will be dispersed to greater distances than megaspores.
as
We under calm con-
investigated aspects of spore size and sculpture as well as spore dispersal
We
ditions and under the effect of artificial wind of some Selaginella species. found that differ-
ences between the species existed that were correlated with active or passive release of micro-
and megaspores. The dispersal efficacy changed drastically under the effect of wind, showing
between
There was no support the hypothesis of synaptospory
species. for
3
and
Evidence suggests that active spore dispersal
active dispersal.
ig
may
outbreeding. More detailed investigations reveal species specific corre-
3
gametophytes evolved independently in different
Heterospory and dioecy of
and male
megaspores
The female
separation of
clades of the pteridophytes.
wind
homosporous,
microspores changed the conditions of spore dispersal. In
much
distance
being transported a certain is
dispersed ferns the probability of
wind
pteridophytes
Assuming heterosporous
the same each spore. that in
for
and microspores are likely to
dominant, the smaller lighter
dispersal
is still
megaspores (Tryon
and heavier
be dispersed longer distances than the larger
to
male and female gameto-
and The distances of
Lugardon, dispersal
1991).
Because
production of spores.
the
phytes thus Heterospory also affects
differ.
number megaspores per individual
of
of higher energetic investments, the
and
number microspores (Tryon
of
plant reduced comparison to the
in
is
heterosporous pte-
ecology of
As consequence, the dispersal
Tryon,
1982). a
homosporous (Cousens, 1988).
ferns
from of
ridophytes that
likely to differ
is
and
widespread contains
Beauv.
The heterosporous genus Selaginella is
P.
spore dispersal
numerous The efficacy of their active
1990).
species (Jermy,
He showed mega-
the
that
by Goebel
mechanisms was (1901).
investigated
first
manner from the micro-
quite different
megaspores
sporangium the in a
ejects
He
gave a
microsporangium (Goebel, 1901).
mechanism
spore release of the
was
recently
mechanism megaspore release that
of
detailed description of the
mechanism was
megaspore discharge
The
rediscovered by Page active
(1989).
by
Studies Straka
(Page, 1989).
termed "compression and slingshot ejection"
Author correspondence.
for
'
VOLUME NUMBER
FERN
JOURNAL:
87
3 (1997)
Somers and Koller and Scheckler (1986) revealed that variations
(1962), (1982),
mechanisms microspores Passive spore release as well as
in release of exist.
active spore release were found. Both types can occur under conditions of
movements
due sudden micro
calm or wind. Active spore release to of the
is
sporangium walls caused by changes of the cell turgor during desiccation.
A
namely syn
possible function of spore sculpture in respect to dispersal,
was emphasized by Kramer Primary synaptospory means
aptospory,
(1977).
'
away
that diaspores are dispersed together straight from the source
]
whereas secondary synaptospory describes the sticking together of diaspores
may
after the dispersal of single spores. Spore sculptures enhance synaptos
A
may
pory. special type of synaptospory be found in heterosporous ferns,
i.e.
and
the dispersal of units consisting of micro- megaspores.
The
ecological consequences of the different above-mentioned spore release
and dispersal mechanisms have not yet been studied. In the present investi
We
we
compare
gation the spore dispersal of five species of Selaginella. ad
dress the following questions: Are there morphological characteristics of the
1)
and
micro- megasporangia and/or the micro- and megaspores support
that dis
mechanisms? Do
modes?
persal 2) the species differ with respect to release 3)
Do
different release mechanisms of micro- and megaspores result in differ-
How
ences in dispersal distances? do these distances change under the
4)
wind?
effect of Does primary synaptospory between micro- and megaspores
5)
Methods
and
Materials
The
Species.—The
following species cultivated in the Botanical Garden of the
University Zurich were
of
investigated: Selaginella anceps
(C. Presl) C. Presl,
kraussiana
S. A. Braun, lepidophylla and
S. Spring, martensii Spring,
S. S.
pallescens The
(C. Presl) Spring. species were identified using Vareschi (1968)
and
Alston
et (1981).
al.
Morphological
Traits of Sporangia and
Spores.—The
diame-
size (largest
and
ter) the surface sculpture of the outer spore wall of micro- and megaspores
were
determined
using a microscope and SEM.
light Sizes of both spore types
were measured
roughly;
a measurement was
statistically relevant spore
of sizes
not intended. The arrangement
of micro- and megasporangia on morphological
units of plants below) was
(see determined
using microscope.
a dissecting
Sporangial arrangement
of each was
species assigned to the four types given
by Horner and
Arnott Type
(1963). basal megasporangiate zone and superior
I:
microsporangiate zone; Type two rows
megasporangia and two rows
of of
II:
microsporangia
within each
Type
strobilus; with two rows mi-
IP: strobili of
crosporangia and two
rows
containing both mega- and Type
microsporangia;
wholly
megasporangiate
III:
strobili.
Spore Release.—The
opening
of sporangia and manner
and
the of active pas-
sive spore were
release observed
visually in all five species under a dissecting
FILIPPINI-DE GIORGI ET DISPERSAL SELAGINELLA
AL.: IN
—
we
Spore Dispersal. Because of the branching morphology of Selaginella,
used morphological These were
units of plants as spore sources. vertically
cm
oriented, frond-like parts of shoots about 40 long in anceps,
fertile S. S.
and The were
martensii, pallescens. units short, horizontally oriented
S.
shoots of lepidophylla and short, horizontal parts of shoots with some erect
S.
As were
strobili in S. kraussiana. a consequence, the spores not released at
even heights in experiments. This experimental design was chosen in order
all
under
to get an impression of the pattern of spore dispersal distances natural
conditions.
We
arranged two types of experiments, one in calm and one with moderate
Room
wind. Both experiments were carried out in a calm room. temperature
was constant 20°C, which allowed slow desiccation of the morphological
at
The room was
units, a basic requirement for spore dispersal. floor of the cov-
ered with black paper.
Morphological units bearing ripe micro- and megasporangia of S. anceps, S.
an
martensii, and pallescens were placed erectly with the strobili at ap-
S.
cm
cm
proximate 30 above Eight rows, each of 59 length, of
height of surface.
were
microscope covered with double-sided clear sticky tape laid at
slides
angles of 45° around the spore source. The experiments were conducted for
microspores
twelve hours. Then, the diaspores (single microspores, tetrads of
were counted each centimeter of each row on an area
or single megaspores) in
of 16 mm^ under a light microscope. The numbers of diaspores were extrap-
cm
and mean per distance from the spore source of the
olated cm^, the
to 1
rows was For kraussiana and S. lepidophylla, a similar
eight calculated. S.
much
morphological
smaller
experiment was performed, but because of the
cm
3-4 above the surface), they
a height of
units of these plants (strobili at
and rows around the spore source
were boxes, the 8
carried out in large plastic
had
a length of 14 cm.
and
We
kraussiana,
spore dispersal of anceps, S. S.
also investigated the S.
morphological units of these
wind. Again,
martensii under the influence of
with dou-
rows microscope slides
species were placed in a calm room. Five of
cm 45°
were angles of in a
each 119 long, laid at
ble-sided clear sticky tape,
On
small
the other side, a electric
semicircle on one side of the spore source.
= cm) was
propeller 19
propeller (Konig AG, Ziirich, type 316; diameter of the
wind
placed m. This propeller did not produce a linear flow,
a distance of 1
at
which we be more representative
believe to
but an with turbulence,
current
air
wind The wind speed was measured at the position of
for natural conditions.
Grant Ltd., Britain). In all
the strobili using a digital data logger (Squirrel,
The
m/s was
mean wind speed of 1.16 adjusted. ex-
experiments moderate
a
was
Data analysis carried
twelve hours.
periments again were conducted for
out in the manner described above.
checked eventual synap-
were for
Synaptospory.— experiments careftilly
All
tospory between micro- and megaspores.
VOLUME NUMBER
AMERICAN FERN JOURNAL: 87 3 (1997)
96
Table Morphological characteristics of microspores, megaspores, and strobili of Selaginella anceps,
1
.
Arrangement
and pallescens used dispersal experiments.
S. kraussiana. S. lepidophylla, S. martensii, 5. in
of sporangia within strobili according to Homer and Amott (1963; for explanations see text).
Surface of micro- obtuse cones ely prickly papillate
spores
~300^tm
(with flange)
Surface of mega- with large equa-
spores flange
torial
spores
passive
spores
Arrangement of spo- type
I
Results
Characterization of Micro- and Megaspores.—The
investigated species of
Selaginella had megaspores were 6-16 times diameter than the
that larger in
dispersal units of the microspores, single microspores or microspore
tet-
i.e.,
The
rads (Table megaspores were found kraussiana 620
largest in
1). S. (ca.
ixm in diameter). In anceps, lepidophylla, and martensii microspores
S. S. S.
were
dispersed as tetrads (Table Selaginella kraussiana dispersed single
1).
microspores, whereas in S. pallescens both single microspores and tetrads oc-
noteworthy
curred. It is that the single microspores of S. kraussiana approxi-
mately reached the size of the microspore tetrads of the other species.
The
surfaces of both types of spores showed distinct characterizations (Table
1, Fig. 1). In S. anceps, the megaspores were characterized by a large equatorial
The
flange. microspores of S. kraussiana were extremely spiny. In lepido-
S.
phylla, the surfaces of the microspore tetrads had burlike structures the
at
seemed
edges be complementary
that to to the feltlike surfaces of the mega-
A
was
spores. similar case found in martensii, but here the microspore
S.
were
two
tetrads finely prickly. In of the investigated species, surface struc-
tures of the spores were documented, which
principally allowed synaptospory
between and
micro- megaspores, whereas
the surface structures of spe-
five
all
allowed synaptospory
cies of microspores. In the dispersal experiments (see
GIORGI ET DISPERSAL SELAGINELLA 97
FILIPPINI-DE AL.: IN
we
below), sometimes observed groups of microspore tetrads dispersed as one
We
Arrangement and Megaspqres Within the Strobili.— found
of Micro-
by Horner and
three of the four types of sporangial arrangement described
occured
Arnott Type with megasporangia at the base of the strobilus,
(1963).
I,
and Type with
anceps. entirely vertical
kraussiana, martensii,
in S. S. S. II,
was documented
rows of either micro- or megasporangia, in S. lepidophylla,
was
and with but intermingled rows of both sporangial types,
type
vertical,
IV,
found
in pallescens.
S.
morphological
The usually were oriented within the plane of the
strobili
the shoot (Table Depending on the architecture of the species, the
unit,
1).
i.e.,
observed
sporangia were oriented vertically or horizontally, the latter
strictly
with
kraussiana, tower-like
in strobili.
S.
Spore Release.—The height above surface at which the spores were released
The
changed among the species and clearly affected the dispersal distances.
cm
above
were only
kraussiana and lepidophylla at heights of 3
strobili of S. S.
surface (Table
1).
passively dispersed (Table In S.
Microspores were either actively or 1).
preformed dehiscence
microsporangium opened along a line,
kraussiana, the
and
described in Koller
and microspores were passively dispersed (as
the
opened during desic-
wall
The two valves of the sporangial
Scheckler, 1986).
were exposed
The microspores to
remained open.
Subsequently, they
cation.
on the inner surface of the
secretion
the and, as a consequence, the tapetal
air
by wind.
Some and some were dispersed
spores out
valves
dried. fell
spores actively
The microsporangia of the other four species dispersed their
end and continued
open
The sporangium started to at the distal
(Table
1).
microsporan-
The two valves of the
opening along a preformed dehiscent line.
When between the
the angle
backwards.
spread and borders bent
gia their
dispers-
sporangium suddenly closed, actively
valves reached about 150°, the
ing the microspores.
sporangmm and
open
megaspores passively out of the
In anceps, the fell
S.
m
an-
mechanism Therefore, S.
(Table
were by slingshot 1).
not dispersed a
were dispersed.
microspores actively
ceps, only the
megasporangium
the
Selaginella,
species of
In the other four investigated
the valves
During desiccation,
by Page
opened manner described (1989).
in the
were then
The megaspores
150° was reached.
spread an angle of about
until
lymg
ones the
the at
megaspores,
The two outer i.e.,
from each
separate other.
corresponding
hollows of the
were both located in
borders of the valves,
boat-shaped basal part of the
The two megaspores were in the
inner
valves.
sprang back into their orig-
movement, the valves
With sudden
sporangium.
a
megaspores (Table
the 1).
ejecting
inal position, actively
spread
sporophylls
megasporangia the
and
During the opening of the micro-
spore
90° even more, leaving space for dis-
approximately or
an angle of
to
45°.
an angle of
they closed again to
After spore release
persal.
VOLUME NUMBER
AMERICAN FERN JOURNAL: 87
(1997)
3
GIORGI ET DISPERSAL SELAGINELLA
FILIPPINI-DE IN
AL.:
—
Spore most megaspores were only dispersed into
Dispersal. In anceps,
S.
wind
experiments without
the close vicinity of the spore source in the (Fig.
mechanism
a result that in accordance to the passive spore release of
2), is
cm^ were found
this species. Densities of 1300 microspore tetrads (Fig. lb) per
cm The microspores landed
within 20 from the source majority of the
(Fig. 2).
known
here, leading the well leptocurtic curve of spore dispersal (Fig. 2).
to
However, a minority was dispersed to distances up to 59 cm. Microspores were
sometimes up 100 This
clumped forming groups of to tetrads.
often together,
seemed to be due mainly to a tapetal secretion on the surfaces of the spores.
Under moderate wind of 1.16 m/s, an almost uniform dis-
the influence of a
The abun-
persal curve was observed, exhibiting no obvious peaks (Fig. 2).
experiment decreased only slight-
dance microspores within the range of the
of
The megaspores reached
also
ly with increasing distance from the source.
wind—
cm experiment with possibly assisted
greater distances—up to 69 in the
by
their large equatorial flange (Fig. la).
experiments
Similar results were obtained for the microspore tetrads in the
we counted about 920 mi-
with Near the spore source,
martensii
S. (Fig. 2).
released
marked anceps, the actively
crospore tetrads per cm^. In contrast to S.
and
calm conditions
distances in
megaspores martensii reached similar
of
S.
Under
cm
under wind up 59 from the spore source.
to
the of
effect (Fig. 2), i.e.,
the results of
calm experiment with pallescens (Fig.
conditions in the S. 2),
found mar-
curves in
micro- and megaspores corresponded to the dispersal S.
above
from the de-
and kraussiana differed
Selaginella lepidophylla S.
view
proximal
Selagmella species,
SEM and megaspores of a)
micrographs of microspores
1
. .
equatona
anceps;
microspore tetrads of S. c)
megaspore anceps with equatorial flange; b)
of
S.
1
proximal
kraussiana;
w spiny microspore of S. e)
of a megaspore of kraussiana; d) single,
S.
proximal view
w lepidophylla;
of a megaspore of lepidophylla; microspore tetrad of S. g)
S. f)
martensn; equatorial
of
microspore tetrad S. i)
megaspore prickly
of martensii; h) finely
i S.
w microspore of pallescens. Scale bars: a. c. e, g,
S.
of a megaspore of pallescens; k) single
S.
=
100 lO^m.
k
|xm; b, d, h,
f,
VOLUME NUMBER
AMERICAN FERN JOURNAL: 87 3 (1997)
I
UmJiua
Ji
n
lllsiiilil
UL
| calm
calm kraussiana
S.pallescens/calm S. lepidophylla / S. /
L__
"Ili^
:Ljli1
[cm] Distance from source (cm]
;
cm
Fig. 2. Dispersal distances in of the percentages of microspores and megaspores of Selaginella
anceps (mean
percentages of three replicates], S. kraussiana (mean percentages of four replicates],
S. lepidophylla (mean percentages of three replicates], pallescens, and martensii in calm or
S. S.
wind
with Note
(1.16 m/s]. different scales of the x-axis.
scribed species in the height of strobiU above ground, which was only about
cm
3-4 The
(Table actively dispersed megaspores of both species reached
1).
cm
distances of at least 14 under calm conditions, but most of the microspore
tetrads in S. lepidophylla (Fig. and most of the spiny single spores in S.
2),
GIORGI ET DISPERSAL SELAGINELLA
FILIPPINI-DE AL.: IN 101
kraussiana were found close to the spore source (up to 2 cm; Fig. In an
2).
experiment with wind, only a few micro- and megaspores were found in
S.
kraussiana and the results are therefore not shown. Because there were ripe
sporangia of both types on the morphological units and because these sporan-
gia were obviously empty after the experiment, one had to conclude that the
cm
much
spiny microspores were dispersed greater distances than the 119
for
experimental
of the setup.
Synaptospory.— experiments
In investigations as well as in the dispersal
all
no primary synaptospory between micro- and megaspores was de-
case of
DlSCUSSION
homosporous viable spore theoretically sufficient to
In ferns a single is
new
new due intragame-
and found population,
achieve sporophyte a to
a to
tophytic (Schneller and Holderegger, 1996). In any heterosporous spe-
selfing
cies a microspore and a megaspore must be placed in close proximity to gen-
new The heavy megaspores,
formation of
sporophyte (Kramer, 1977).
erate a
compared with microspores, clearly reduces the effectiveness of
small, light
As
con-
wind and thus the potential for long distance dispersal. a
dispersal,
primary
heterosporous pteridophytes differ in
sequence, the dispersal units of
be dispersed long
microspores have the ability to for
dispersal distances: the
whereas megaspores are dispersed only locally.
distances, the
two types of sporangia.
of
Heterospory ultimately led to the differentiation
Somers, 1982; Koller
1902;
Earlier investigations (Goebel, 1901; Steinbrinck,
and
morphological, anatomical,
& revealed the
Scheckler, 1986; Page, 1989)
genus Selag-
and megasporangia in the
between micro-
functional differences
present study also
The investigated in the
Selaginella
species of
inella. five
Schneller (1995)
marked the manner of spore release.
exhibited differences in
homosporous
between
occur
showed spore release also
that differences in
ferns.
synaptospory well as sec-
As Kramer primary (as
by
hypothesized (1977),
mechanism assure fertilization
ondary) mega- and microspores could be a to
of
within
genetic variation
the
the case,
in heterosporous pteridophytes. this
is
If
due intergametophytic self-
the progeny would consequently be restricted to
evidence
some morphological in
gave
Kramer and Dahlen
(1990)
ing. (1977)
and megaspores often
micro-
The structures of
favor of hypothesis. surface
this
we
also
our investigations,
seem and key manner. In
lock
to together in a
fit
sug-
spore surfaces that
of the
detected some morphological characteristics
megaspores.
on
would then "ride" ejected
Microspores
gested synaptospory.
and megaspores
between micro-
synaptospory
However, hypothesis of
this
were
and microspores
Mega-
could not be confirmed in our investigations.
dispersed
separately.
a
c
^ SelagineUa
on spore dispersal of i
To our knowledge, no investigations exist
distances (Mitchell,
on dispersal
under Published data
natural conditions.
VOLUME NUMBER
AMERICAN FERN JOURNAL:
87
102 3 (1997]
based on laboratory observations under
1910; Ingold, 1939; Page, 1989) are
we
showed
calm our experiments using wind, that the
conditions. In artificial
more
microspores transported and well spread over distances of than
are easily
m
mean
Compared
from the spore source. to the size of the spores of ho-
1
mosporous ferns (Kramer 1995), the microspores of Selaginella species
et al.,
Wind
are smaller and thus more effectively wind dispersed. also seems to have
on megaspore dispersal especially in the case of the passively
effects (Fig.
2),
which by
dispersed megaspores of anceps, are characterized a large equa-
S.
would than
microspores disperse greater distances
torial flange. In nature, far
megaspores under the influence of wind, turbulence, and squalls. Long dis-
tance dispersal of microspores thus increases the probability for outbreeding.
wind
Active mechanical dispersal and dispersal are not mutually exclusive.
The wind by
former can additionally faciliate dispersal. Active spore release
megasporangium would enhance
the further the possibility of cross
fertiliza-
when
tion, especially in calm, the majority of microspores are deposited ad-
and megaspores
jacent to the source (leptocurtic dispersal curve; Fig. the
2)
dispersed This megaspore mech-
are greater distances. effective active release
may new
anism
also increase the probability for the establishment of sporo-
due among
ph5^es decreased competition
to siblings.
may
Secondary synaptospory after spore dispersal be relevant in promoting
The complementary and mega-
fertilization. spore surface sculptures of micro-
A
spores possibly play a role in the effectiveness of secondary synaptospory.
group
of fertile microspores or a group of microspore tetrads in the vicinity of
may
a megaprothallium enhance
significantly the probability of fertilization,
because of higher number spermatozoids Water and
of
its that are released.
may
electrostatic effects also play a role in secondary synaptospory.
We
know much
do not about the breeding systems of Selaginella species,
especially in natural populations. Simple breeding experiments showed
that
martensii formed
S. frequently viable sporophytes through intergametophytic
selfing (Filippini-De Giorgi, unpubl. data). In an electrophoretic study of some
populations
of S. helvetica in Switzerland, considerable genetic variation
within and among was
populations found (Holderegger and unpubl.
Schneller,
We
data). believe that dispersal an important but unfortunately neglected
is
part of the life cycle in studies of population biology of pteridophytes. Our
preliminary study on
the dispersal biology of heterosporous Selaginella spe-
many
cies reveals possible correlations between morphology, sculpture
surface
of the outer spore
wall, ecological determinants drought wind, breeding
like or
and
system, population
genetics. Further, thorough studies should include the
determination
of the terminal
settling velocities of either spore type (see Nik-
las, 1992) or experimental designs allow an
that
investigation of lateral dis-
from
persal out
a real point-source The
a single data gathered
(i.e., strobilus).
in our experiments had low
statistical power. Therefore, large sample size ex-
periments
of spore dispersal under
strictly controlled conditions, perhaps in
wind
a tunnel, are needed.
Investigations of additional species using different
may
methods
whether
reveal inbreeding and
outbreeding occur natural pop-
in
whether
ulations, differences in the breeding system between
species exist.