Desiccation and Rehydration Experiments on Leaves of 43 Pteridophyte Species

2007·6.2 MB·English

by  Michael Kessler

American Fern Journal 97(4):175-185 (2007)
on Leaves
Experiments of
and Rehydration
Desiccation
Species
43 Pteridophyte
and Yvonne Siorak
Michael Kessler
Systematische Botanik,
Pflanzenwissenschaften, Abt.
Albrecht-von-Haller-Institut fur
Germany
Untere Karspule D-37073 Gottingen,
2,
We and rehydration experiments on the detached leaves of 43
Abstract.— conducted desiccation
among
pteridophytes.
drought adaptation strategies
pteridophyte species to assess the variability of
homoiohydric
We responses from poikilohydric to strategies
found complete grades of desiccation
mesomorphism xeromorphism. These results suggest that
and within the category from to
latter
wide drought adaptation strategies
pteridophytes have repeatedly evolved a variety of
not adequately
(poikilohydry and xeromorphism at least 12 and 6 times, respectively) that are
between homoiohydry and poikilohydry.
by simple distinction
described
a
mesomorphism, poikilohydry, xero-
homoiohydry,
Words.—
Key drought adaptation strategies,
morphism, rehydration
desiccation,
humid
and habitats
most abundant species-rich in
Ferns and lycophytes are
become
number have
species also
but considerable of
Kessler, 2001), a
(e.g.,
Most
1977; Page, 2002).
adapted arid conditions (Pickett, 1931; Gaff,
to
mesomorphic and without any special
pteridophytes can be characterized as
show
numerous variety of
However, taxa a
drought
adaptations to stress.
These adaptive
drought and desiccation (Table
adaptive strategies to stress 1).
and
detailed
plant physiologists,
have long attracted the attention of
strategies
number
M
Chamb
and
Quirk
Asplenium ceterach (Rouschal, 1938),
L.
riomes 2003),
•,
and Pleopeltis poly-
particular
Polypodium vulgare (Kappen, 1964), in
L.
Andrews & Windh. and (Pessin, 1924, 1925;
relatives
podioides E.G. its
(L.)
on with
These focussed taxa
studies
1968; Miiller et al, 1981).
Stuart,
poikilohydry,
conspicuous water drought adaptations, especially
particularly
and physiological
phylogenetic
and covered only small range of the
a
no
currently
and Accordingly, there
within lycophytes. is
ferns
variability
sampling of drought adaptation strategies for
taxonomically representative
documented 19
been in
example, poikilohydry has
For
pteridophytes.
12
pteridophyte genera (Proctor and Pence, 2002), belonging to at least
phylogenies of
recognized in the
independent evolutionary lineages as
The morphological,
and Smith anatomical,
Schneider (2004) et al. (2006).
et al.
among
mechanisms involved poikilohydry differ several
and physiological in
mechanisms
A
conspicuous example of contrasting is
of these lineages.
by
rehydrate
with one-cell-thick leaves that
presented by the filmy-ferns their
and
polypodioides
and
1940 Pleopeltis its
water contact (Hartel, b)
direct a,
CD
Table
Several plant adaptive
1. strategies to counter drought and among
stress, their representation pteridophytes (modified from
Levitt, 1958;
Benzing, Losch, The
1990; 2001). lower
five categories together form the group homoiohydric
of
strategies.
Reaction
of leaves Reaction
of leaves
Strategy Morphological and
phenological
characters
to desiccation rehydration
to Fern taxa (examples)
Poikilohydric
an
rapid; leaves up; up rapid
roll full recovery; cheilanthoids,
when
rehydrate water 95%
is available, often to water loss water uptake through Hymenophyllum,
densely
scaly
possible without
leaf surfaces Pleopeltis and
allies,
lethal effects some
Selaginella
Mesomorphic
leaves of intermediate
thickness,
soft to rapid; leaves wither slow; water content most
ferns
hard, sensitive to desiccation; no special and >
strongly develop
does not or very
J
adaptations drought
to stress
necroses
after slight slowly recover
to
water 2
loss
original levels
n
Xeromorphic
leaves thick, hard, narrow,
often
slow; leaves maintain slow; water uptake some Asplenium, Campv- >
longitudinally folded or rolled, with shape and z
their mostly through
loneurum, some
roots
abundant
sclerenchyma;
leaf surfaces
thickness; survive
Elaphoglossum,
waxy
with
a cover; stomata abundant,
moderate water
loss Niphidium, some z
sunken
into the leaf surfaces; venation
podium
Poly
o
density high
c
Succulent
leaves or rhizomes thick and spongy, become
slow; leaves slow through Lemmaphyllum, z
leaves;
strongly change >
their thickness
in thinner as they water uptake mostly
Pyrrosia
response
hydration
to status dry out and survive through 9 -
roots
<
high water
loss
Drought-
leaves, pinnae, or pinnules are shed in the rapid unknown
to intermediate; some Adiantum,
deciduous medium
dry season, thin
to thickness
leaves, pinnae, or
Nephrolepis,
pinnules shed
are
Phlebodium
under water
stress
Z
Impounding
leaves arranged in a funnel; water not unknown unknown C
is some Asplenium
impounded
directly as in bromeliads,
but mostly stored accumulated
in organic
material
vi
REHYDRATION PTERIDOPHYTE SPECIES
DESICCATION & IN 43 177
KESSLER & SIORAK:
adapted epidermal scales (Miiller
h specially
from poikilohydric
to
transition
1981). In other cases, a full
et
al.,
For
been documented within a single species.
homoiohydric behavior has
omoio
summer
lm
wide spectrum
hide of
drought adaptations (Table a
these contrasting stress 1)
and Tuba,
mixed 2002).
(Proctor
intermediate, or strategies
different,
and biased sample of studies of
physiologically
Given taxonomically
the
among pteridophytes, the aim of the present
drought adapation strategies
among
drought strategies
study was assess the variability of stress
to
and rehydrating excised leaves
by experimentally desiccating
pteridophytes
belonging
from 43 pteridophytes
stem sections in the case of Selaginella)
(leafy
Our
taxonomic groups and morphological types. basic
wide range of
to a
could be distinguished
was adaptive strategies
assumption that the different
This applies
and rehydration (Table
desiccation
by the reaction of leaves to 1).
Wat
mo
between poikilohydric taxa capable of
can only distinguish
excised leaves
doing
and homoiohydric taxa incapable of so.
through leaves
water absorption
provided insights into
the study of detached leaves has reliable
Historically,
and due
the
and Golovina, 2002) to
(Leprince
plant physiology in general
method
whole has been the of choice
and weighing plants,
drying
of
difficulty
and
Pickett
with 1924, 1925;
experiments ferns (Pessin,
desiccation
for
Manuel
Q
1981;
Miiller et
al.,
Methods
Material and
stem
Gottingen,
Garden University of
Botanical of the
collection of the
living
Germany
adaptations
an obvious variety of to
on groups exhibiting
with focus
forms, a
1*
A "1
mesomor •m • 1 4 1 I
and
one water-impounding, 12 in-
two drought-deciduous,
xeromo
mat
An was species
intermediate category established tor
termediate species.
mesomorphic xeromorphic
or
could not be unambiguously placed in either the
No were study.
succulent species available for
categories.
pinnae the case of
were conducted with excised leaves, (in
Experiments
water content of fully
Total
stem section [Selaginella).
large fronds), or
Freshly
experiment.
was determined prior the desiccation
hvdrated leaves to
were hydrated by wetting their
from well-watered plants fully
cut leaves
em
ambient temperatu
mas
determi
Table
Desiccation
2. resistance, desiccation and
delay, recuperation capacity
of excised leaves from 43
species
of pteridophytes.
Letters in brackets
names
after the indicate wether whole
leaves pinnae stem
(L), (P). or sections (S) were studied.
Morphological
Desiccation
resistance Desiccation Recuperation
capacity
Species
categorv (% water
contents) delav (hours) (% water
contents)
Adiantum
capillus-veneris
L. (L) deciduous
81
2 87
Adiantum
macrophyllum
Sw.
(L)
intermediate
99
4 59
Adiantum
trapeziforme
L. (L) mesophytic
51
2 84
Adiantum
villosum
L. (L)
intermediate
86
3 100
Anemia
mexicana
Klotzsch
(L)
poikilohydric
74
2 75
Anemia
rotundifolia Schrad.
(L)
poikilohydric
86
3 90
Anemia
tomentosa
Sw.
(Sav.)
(L)
poikilohydric >
99
4
67
Asplenium
bulbiferum
G. Forst.
(L) xerophytic
73
6 84
Asplenium
daucifolium Lam.
(L)
intermediate
86
6
54
Asplenium dimorphum n
Kunze
(L)
intermediate
65
>
6 78
Asplenium
mannii Hook.
(L) mesophytic
30
82
1
Asplenium marinum
L. (L)
intermediate
81
3 76
Asplenium
nidus
L. (L) impounding
58
7 57
Asplenium
Kunze
rutaefolium
(L) intermediate
75
5 80 c
Asplenium
salicifolium
L. (L)
intermediate
80
7 68
Blechnum
brasiliense Desv.
(P) mesophytic
47
86
Blechnum
cordatum
(Desv.) Hieron. >
(P) mesophytic
59
90
1
Blechnum
occidentale
L. (L) mesophytic
68
96 <
1
Blechnum
spicant Roth
(L.) (L)
intermediate O
81 4 —
55
Campyloneurum
xalapense Fee
(L) xerophytic
81
7 74
Cheilanthes
myriophylla
Desv.
(L)
poikilohydric
99
6
38
Cheilanthes notholaenoides Maxon
(Desv.) ex Weath.
poikilohydric
(L)
85
5 96
Elaphoglossum apodum
(Kaulf.) Schott ex Sm.
mesophytic
(L)
60
J. 4
59
Elaphoglossum
crinitum
Christ
(L.) (L) mesophytic
C
63
2 49
Elaphoglossum
engelii
(Karst.) Christ
(L) xerophytic
44
7 75
Elaphoglossum erinaceum Moore cc
(Fee) T. mesophytic
(L)
74
2 66
Elaphoglossum
latifolium (Sw.) Sm.
(L) intermediate
74
J. 6 49
Hemionitis
(Burm.) Moore
arifolia
T.
(L) poikilohydric
96
4
7o
^j
7^
8°
CO
O
>
Table Continued.
w
2.
n
Recuperation
Morphological Desiccation resistance Desiccation capacity n
>
category (% water contents) delay (hours) (% water contents)
Species
96 13 91
palmata poikilohydric
Hemionitis
L. (L) Z
Microgramma poikilohydric 95 6 35
piloselloides Copel.
(L.) (L)
80
Pecluma M.G. poikilohydric 91 4
eurybasis (C. Chr.) Price (L)
64
deciduous 72
Link 1
Pellaea sagittata (Cav.) (L)
47
intermediate 91 6
Polypodium Fee a
australe
(L)
36 49
Hook & xerophytic 70
Polypodium scouleri Grev. (L) >
H
100
Polystichum lachenense (Hook.) Bedd. intermediate 89 2
(P)
O
mesophytic 74 4 72
Polystichum platyphyllum (Willd.) C. Presl (P) z
mesophytic 46 99
2
Pteris quadriaurita Retz. (P)
z
83
mesophytic 86
Selaginella geniculate (C. Presl) Spring (S) 3
99 63 CO
Link poikilohydric 2
Selaginella helvetica (L.) (S)
a
mesophytic 67 93 H
2
Selaginella martinensii Spring. (S)
56
mesophytic 88
2
Selaginella rotundifolia Spring. (S)
poikilohydric 90 4 58
Aspl.
Selaginella trisulcata (S)
G
86
mesophytic 69
Selaginella vogelii Spring. (S) 1
H
M
n
cc
AMERICAN FERN VOLUME NUMBER
1»0 JOURNAL:
97
4
(2007)
C
105 weight constancy was
until achieved. Total water content was then
calculated by mass
subtracting dry from
its the fully hydrated mass. In the
and
actual desiccation rehydration experiments,
different fully hydrated
leaves (see above) were placed in a drying oven at 40 C for 20 different time
periods
(0.5, 1, 2, 3, 14, 15, 18, 24, 30, and 36 hours) and weighed
...,
afterwards. These leaves were then wetted and placed closed
in plastic bags
for
one
to three days until reaching weight constancy. Water and
loss absorption
were
expressed
as the percent value of the total water content of leaves each
for
species. Leaves were considered be damaged when 50%
to lethally
at least of
showed
the lamina made
tissue necroses. Replicates each) were only
(five of
three species {Aciiantuni capillus-veneris L., BJechnum brasiliense Desv., and
mo
We
calculated the following parameters: desiccation
resistance, the
percentage
of the total water contents that could be lost before leaves were
damaged;
lethally desiccation delay, the time until the leaves became
lethally
damaged;
recuperation capacity
(resatu ration), the percentage of the original
water contents that was regained at the point of desiccation resistance.
RlvSDLTS
me
Table For example,
(Fig. lethal desiccation were reached
1, 2). levels
in
different species after 1 to 36 hours and water losses of 30-99%,
at as
determined from the desiccation delay and
desiccation
resistance parameters,
respectively (Table was not possible discern groups
2). It to distinct of species
could
be assigned
that to specific drought adaptation
strategies
(Fig.
2).
Because
excised pinnae stem were
or sections only used
for a few, usually
related species (five and six species, respectively), no formal was possible
lest
whether
of these samples
differed systematically from species studied with
entire leaves, but visual inspection of the results show no apparent
trends.
The
three species with measurements showed
five replicate each
re-
producible with measurements
patterns, having on average
a coefficient of
much
12%, which
variation of lower
than the variation observed between
is
species (54%).
Discussion
To
our knowledge,
this is the first study to compare the desiccation and
rehydration behavior number
of a large of pteridophyte species with
consistent method.
a In the interpretation of the results should be borne
in
it
mind
experiment was
that the conducted on detached and
leaves, that the
absolute values of the dehydration behaviors therefore do not correspond
to
the values and
of entire intact living plants. This especially
relevant the
is for
ability of the plants rehydrate, because
to of the difficulty of accurately
determining
the health status of leaves based only on
external visual
As
examination. a result of using excised some were
leaves, leaves
certainly
REHYDRATION PTERIDOPHYTE SPECIES
181
KESSLER & SIORAK: DESICCATION & IN 43
Ad Adiantum
anturn
i 100 100
100
capilluS'Veneris villosum
80
80
60
60
40 40
20-
20
»
.
6 g 12 6 9 12
100
100
100
'
palmata
Elaphoglossum Hemionitis
Cheilanthes 100-
100
100 100
\
i
myriophylla folium
lati
80-
80
80
Campyloneurum s
60
c 60
60
CD
.
xalapense
40 40
40
o
o
20 -
20
20
J L X - ^
1 i I
6 12
6 9 12 6 9 12 6 9 1?
T
\ Pedum
Microgramma J a eurybasis
100
_
100 100 V 100
pHoselloides
80
80
60 60
\ <
V
\
40 \^ 40
*s
\
20 20
1
s
\
•<-\
r\ 1 i .i_ . -
6 9 12 6 9 12
Polystichum
100
100 100 100
platyphyllum
80
60
40
20
6 9 12
time
(h)
pinnae stem sections
and rehydration responses of detached leaves, or leafy
Desiccation
Fig.
1.
were chosen represent the range of
Species to
pteridophyte species.
20 selected
Selciginella) of
(in
Dashed show water
the
and rehydration experiments. lines
observed responses to the desiccation
when continuous represent the water content after redydration.
content desiccated, lines
1H2 AMERICAN FERN JOURNAL: VOLUME NUMBER
97
4 (2007)
poikilohydric
100 *
v
*
myriophylla
C.
helvetica
S.
palmata
H.
•
•
CD
xalapense
O
C.
80
t
E. folium
lati
03 t
scouleri (36h)
P.
70
•
(f)
if)
CD
60
xeromorphic
A
n/dt/s
O
50
CD
O
P. quadriaurita
O 40
mannii
A.
Q 30
mesomorphic
20
10 15
Desiccation delay
(h)
Desiccation
Fig. 2. resistance versus desiccation delay of 43 pteridophyte Deciduous
species.
species are indicated by triangles, the water-impounding species by a squares, and species of
Anemia
by small arrows. remaining
All species are indicated by circles. For the sake of only
clarity,
some
distinctive species mentioned
in the text are labelled with names.
more
damaged
severely by handling
the than
others, affecting their
re-
cuperation capacity. This
evident where,
is in Fig. Cheilanthes
1, e.g.,
myriophylla showed wide
a variation of measurements, suggesting some
that
individual leaves might have been more damaged A
strongly than
others.
general pattern observed most was
for species the gradual decline
in
desiccation and
resistance
recuperation capacity with
increasing
desiccation
The
time.
of these declines
first clearly reflects the gradual loss of water over
whereas
time, the second one presumably
reflects the physiological
or
anatomical damage due
and
longer
to stronger desiccation reduces
that the
ability of the leaves
to rehydrate. Despite these unavoidable methodological
shortcomings,
the present study comparable
previous
to desiccation
is
experiments
with used
ferns that also detached leaves
(Pessin, 1924, 1925;
and Manuel,
Pickett
1926; 1931; Rouschal,
Iljin, 1938; Hartel, 1940
a, b;
Kappen,
1964; Stuart, 1968; Midler Quirk and
et ai, 1981; Chamber,
1981;
Proctor, 2003).
REHYDRATION PTEKIDOPHYTE
KESSLER & SIORAK: DESICCATION & IN 43 SPECIES 183
and
high gradual
Perhaps the most important result of our study is the
among
the responses desiccation and rehydration the species
inability in to
Some showed could be
examined. species patterns that easily attributed to
Examples included Asplenium mannii
drought adaptation
"classic" strategy.
a
water
(mesomorphic) that died quickly after relatively limited loss of (30%),
most
Hemionitis palmata (poikilohydric) that survived loss of (96%) of its
and
water and tolerated desiccation for a long period of time (13 hours),
Polypodium (xeromorphic) dried out most slowly (desiccation
scouleri that
= showed and
delay 36 hours). However, most species intermediate patterns
and
considering species together there were complete grades of desiccation
all
homoiohydric and within
rehydration responses from poikilohydric to species
The
mesomorphic xeromorphic
from species. cline of
the category to
latter
been documented within
mesomorphic and xeromorphic behaviors has also
Kappen
by
single species (1964).
we
As an example of variability within a given drought adaptation strategy
can compare the poikilohydric taxa Anemia and the cheilanthoid ferns
One Anemia been shown
has experi-
{Cheilanthes Hemionitis). species of
,
and
and our
mentally be poikilohydric (Proctor Pence, 2002), field
to
shows
number these
experience with of other species in Bolivia also that
a
and
up under drought
behave as poikilohydric species: their leaves roll stress
by
become and brownish, but the plants can be readily rehydrated
brittle
(M
experiment
much and
had lower desiccation resistance
arrows
black in Fig. a
2)
which well-documented be
desiccation delay than cheilanthoid ferns are to
and
Quirk
poikilohydric (Pickett and Manuel, 1926; 1931; Hevly, 1963;
Iljin,
we
Among
Chamber, unambiguously poikilohydric species
the
1981).
74-99%
measured water losses (desiccation resistance) of (Table This
2).
corresponds well with previous studies which have documented values of up
95%
94% water Notholaena marantae R. Br. 1931), in
to loss in (Iljin,
97% and
polypodioides
Polypodium Pleopeltis
vulgare (Losch, 2001), in
(M %
1938).
two
Looking with unusual the desiccation behavior of the
taxa strategies,
at
deciduous species [Adiantum capillus-veneris, Pellaea sagittata; triangles in
mesomorphic
and
was intermediate between poikilohydric species.
Fig.
2)
low
The difference between these groups therefore found in their response to
is
pinnae
water content, with deciduous species shedding their leaves or
leaf
when There some species with mixed poikilohydric/
they are too dry. are also
Windham. Our
deciduous such Argyrochosma nivea field
strategies, as (Poir.)
Andes shows beginning
experience with species in the Bolivian that at the
this
wet
of the dry season dried-out plants can be readily rehydrated in plastic
had
Several months the end of the dry season, leaves apparently
bags. later at
naked
died and pinnules had been shed, leaving only the rachises (M. Kessler,
know
would deciduousness pteridophytes
be interesting to in
pers. obs.). if
It
from
associated with an active recovery of nutrients or assimilates the
is
AMERICAN FERN VOLUME NUMBER
184 JOURNAL:
97
4 (2007)
which would
leaves, represent a distinct advantage over mesomorphic species
that loose all tissue once the leaves are too dry. Considering the other unusual
impounding
strategy, the only species, A. nidus, behaved xeromorphic
like
taxa.
In conclusion, our study confirms the notion of Proctor and Tuba
(2002) that
plants have evolved a wide variety of drought adaptive
strategies that are not
adequately described by a simple distinction between homoiohydry and
The number
poikilohydry. which
large of cases in poikilohydry has
independently
evolved
in pteridophytes, 12 times and more
at least likely
may
often, suggests that different physiological mechanisms have been
A
developed same
to achieve the adaptive response. similar case can be made
xeromorphic which
for adaptations, appear have evolved independently
to
at
A
dozen
least half a times (M. Kessler, unpubl. comparative study
data). of the
adaptive
efficiency of these different evolutionary cases might yield interesting
insights into the physiological constraints and among
possibilities present
pteridophytes.
ACKNOWLEDGEMENTS
Wo
thank Leuschner and
G. D. Hertel, Dept. of Plant Ecology, Univ. of Gottingen. providing
for
laboratory and M. Schwerdtfeger and
facilities, the gardeners of the Botanical garden of the Univ.
of Gottingen for providing plant material. Ruth Kirkpatrick, Kluge, and two anonymous
Jiirgen
reviewers provided useful comments on the study and manuscript.
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