Turion Overwintering Of Aquatic Carnivorous Plants
Lubomír Adamec, Academy of Sciences of the Czech
Republic, Institute of Botany
Keywords: ecology: Aldrovanda vesiculosa, Utricularia
Overwintering buds (turions; Latin turio=shoot) are vegetative
dormant organs produced by perennial aquatic plants. Turions are formed
in subtropical to polar zones as a response to unfavorable ecological
conditions, and protect fragile plant shoots from freezing and decaying.
Turions are modified shoot apices. Both morphologically and physiologically,
turions of free-floating aquatic plants, and especially of Utricularia
and Aldrovanda, are the most modified ones of all. During the
winter they separate from the mother shoot, which totally decays afterwards.
Turions of aquatic carnivorous plants are more or less spherical, sturdy
organs 1-20 mm in size, and form by the extreme condensation of very short
modified leaves in the shoot apex at the end of the growing season (Figure
1). Their leaves bear only rudimentary traps. Turions are frost resistant,
but their main ecological function is to sink to warmer water. At the
end of winter they rise to the water surface where they sprout in warmer
water. They also behave as propagules and are spread by waterways or water
Initiation and Ripening of Turions
In central Europe, turions formation is preceded by the production of
distinctly shortened internodes in late August. The turions are usually
formed in September after the growth rate of shoot apices reduces. Cooler
and shorter days induce turion formation. N or P deficiency in water apparently
does not have the influence on turion formation of aquatic carnivorous
plants that it does on duckweeds. The relative importance of temperature
decrease and short days probably differs in different species. In U.
vulgaris in Canada (52° N), turions begin to form as early as
August as a result of cooling waters and shortening day length.
Figure 1: Aldrovanda vesiculosa turions stored in refrigerator
over winter, late April 1997.
In thermophilous Aldrovanda, low water temperature is crucial
and decreasing light might be an important effect, but the effect of short
days is negligible. Turions formed about three weeks later (at the end
of September) in Aldrovanda grown in a relatively warm outdoor
culture at Trebon (49°N, Czech Republic) than in plants
introduced to colder shallow waters in the Trebon region (early September).
At the northernmost site at Lake Ladoga in northern Russia (61.5°
N), they form as early as in mid-August and ripen in early September.
In October, Aldrovanda also formed normal turions in a heated greenhouse
where water temperature never fell below 18° C. When grown from turions
in an aquarium on a window ledge in a heated room, normal turions were
also formed in March-May, i.e. under the conditions of long (and increasing)
day length. These plants formed turions in late May after they were transferred
outdoors to colder water. Reports from J. A. Mazrimas growing the Japanese
subtropical Aldrovanda indicate turion formation to be initiated
at 16° C; however, it is not clear whether this is the day, night,
or average temperature. Apparently, turion formation in Aldrovanda
occurs after a long-term marked relative temperature fall (e.g. from 30
to 20° C), and not after reaching some low threshold temperature.
While the formation of turions may occur at 18-20° C, full physiological
turion maturation requires lower temperatures (at least 8-10° C),
lessening light, and possibly also short days. Turion maturation is accompanied
by the translocation of the majority of N, P, and storage organic substances
(sugars) from the dying mother shoots. As turions mature, they become
more compact and contain more storage substances. In the absence of low
temperatures, evergreen shoots do not decay over the winter season but
remain firmly connected to the turions.
The development of turions is also controlled by humic acids. In Aldrovanda,
humic acids in water accelerate the formation, maturation, and sinking
of turions. In spring, humic acids mildly inhibit turions from rising
to the water surface to sprout (by altering their buoyancy); humic acids
also enhance the growth of already germinated turions. Humic acids (and
maybe also tannins) thus play an important role as exogenous phytohormones
leading to optimal seasonal Aldrovanda development.
Sinking of Turions
Figure 2: Utricularia bremii from outdoor culture, late October
1997. Turions are surrounded by baskets of apical leaves. Drawn from
herbarium specimens by E.M. Salvia.
It is interesting that turions of seven similar European aquatic carnivorous
plant species have three different strategies of autumnal sinking and
spring floating. In two strategies, sinking and floating are passive and
are not directly controlled by turions.
a) U. australis, U. vulgaris, U. intermedia, and U. ochroleuca:
in this group, ripe turions are always less dense than water and are firmly
connected to the mother shoots. As the mother shoots gradually decompose,
they become denser than water and drag the turions to the bottom. By early
spring, the turions separate and float to the surface. The turions can
reach the water surface as soon as the ice cover has melted.
b) U. minor and U. bremii: turions start forming in late
August with an unusual structure in the shoot apices (Figure 2). Antler-like
branched leaves form a basket (1-2 cm across) enclosing the developing
turion. In late September and October, light ochre-colored mother shoots
die and drag the turions to the bottom. In autumn the turions break free,
but remain entangled in the apical baskets. They float to the surface
only after the baskets decompose.
c) A. vesiculosa: in this species, a remarkably active way of
sinking and rising has developed. In autumn ripe turions break off the
dying mother shoots at the water surface. After a few days, they sink
gradually to the bottom. Their high density is not only caused by their
high starch content but also, presumably, by their expulsion of excess
gases. In time, the turions are slightly obscured in the sediments. In
April-May, they respond to the warming water, and within a few days rise
to the surface.
Composition and Resistance of Turions
Turions of aquatic carnivorous plants are storage organs. While the dry
weight (DW) of summer shoots is only 8-12% of the fresh weight, it is
25-46% of the fresh weight in autumn. The high proportion of DW in autumn
is caused by the accumulation of starch (25-32 % DW) and free sugars (glucose,
fructose, sucrose; in total 7-14 % DW). Stores of N are in the form of
amino acids (arginine, lysine). Over winter, the metabolism of turions
is very low and probably anaerobic. Their respiration rates at 4-5°
C are about one order of magnitude lower than those of summer shoots at
20° C. Yet, the total content of saccharide energy sources in turions
gradually decreases to 15-24% DW over winter. In this way, the DW proportion
also decreases to about 18-20 %. The spring starch content is rather low
(about 8-11% DW) but the free-sugar content is increased (7-16% DW).
Ripe turions of aquatic carnivorous plants are frost-resistant. Ripe
Aldrovanda turions do not survive storing at -10° C in water
or -12° C in humid air. When they are overwintered in the wet bottom
of a drained tray (our winters are moist so such exposed turions do not
dessicate) or in the field where they are gradually adapted to frosts,
they fully survive frosts of -10 to -15° C. Aldrovanda turions
survive -4° C for long period. U. vulgaris turions exhibit
an increasing resistance to -8° C in the course of winter but they
do not survive -12° C (similar behavior has been observed in U.
australis turions). However, their frost-resistance is very low when
they are germinating. The high resistance of turions to weak frosts of
-2 to -4° C could be used to store them for several years, since turions
survive for only about 10-12 months when stored at 3-5° C. This suggests
turions at natural sites might only survive from one season to the next
one, not longer.
Turions are drought-resistant. In U. vulgaris and Aldrovanda,
turion-like organs are also formed as a result of summer drought. They
are not dormant, and in water, they resume their growth again.
Turions usually overwinter under unfavorable conditions of anoxia, a
strongly reduced medium (i.e. low redox potential), and in the presence
of toxic substances (e.g. H2S or acetic acid). Ripe turions
of aquatic carnivorous plants are able to tolerate these unfavorable conditions
even though experimental evidence for this is still lacking. In the spring,
their tolerance of these conditions decreases.
Dormancy States and Their Hormonal Regulation
After turion formation, two dormancy states can be distinguished. They
are controlled by endogenous levels of stimulating and inhibiting phytohormones.
The dormancy states (and their hormonal patterns) have been described
in detail for Canadian U. vulgaris. Turions enter a state of innate
dormancy at the end of August, when their growth is blocked by endogenous
factors in the turions (even though external ecological conditions are
still favorable to growth). During innate dormancy, aging and dying of
mother shoots (and their sinking to the bottom) occurred. High levels
of abscisic acid (the inhibitory phytohormone) and low levels of free
gibberellins, auxin, and cytokinins, occur this dormancy state. Abscisic
acid has the principal influence, as it induces turion formation. High
temperatures (30° C) can temporarily break innate dormancy, but is
followed by the formation of turions again. Innate dormancy was only broken
by the combination of short days and low temperatures. In field collected
U. vulgaris, this dormancy state was broken as early as in late
October under favorable conditions. In fact, the turion short-day requirement
to break innate dormancy was fully satisfied as early as early September,
whereas the low-temperature requirement was met after 55 days. In Aldrovanda
turions, both in the field and outdoor culture, the short-day requirement
was fully satisfied in early November. Turions stored at 4° C in darkness
germinated at the end of January.
After their innate dormancy, turions of Canadian U. vulgaris enter
a state of imposed dormancy at the end of October. This is maintained
by low, unfavorable temperatures. This dormancy state is characterized
by a decreasing level of abscisic acid and increasing levels of gibberellins,
auxin, and cytokinins. When the imposed dormancy is broken by a temperature
increase, the first turions germinate after two days. Breaking imposed
dormancy begins germination. Low levels of abscisic acid and high levels
of the other three stimulatory phytohormones correspond to this phase.
In Aldrovanda, imposed dormancy breaks at 12-15° C.
Figure 3: Germinating turions of Aldrovanda, early May 1997.
Breaking imposed dormancy (which may not require light) is connected
with the activation of respiration and partial starch conversion to free
sugars. The density of Aldrovanda turions is reduced within 1-2
days so turions rise to the surface where they germinate in of warmer
water, high light intensity, and increasing day length. In duckweed turions,
a small gas bubble (presumably CO2 released from anaerobic
respiration) is produced which pulls the turions to the water surface.
This process can occur in darkness, but is more effective in light. The
density of Aldrovanda turions may be similarly reduced by the production
of CO2 into the fine air spaces in leaves, expelling water
from them. A photosynthetic origin of this gas is unlikely for Aldrovanda.
Moreover, the net photosynthetic rate of dormant turions of bladderworts
and Aldrovanda is very low or negative, even under optimum conditions.
When turions are exposed to light after breaking imposed dormancy, they
resume shoot growth (Figure 3). Although turion germination in itself
is generally controlled by the photoreceptor phytochrome, great differences
in light requirements exist between European carnivorous plants species.
Turions of U. australis and Aldrovanda germinate at higher
temperatures in light only. Those of U. vulgaris, U. minor, and
U. bremii start germinating also in darkness and U. vulgaris
even germinates in the refrigerator at 4° C.
Recent preliminary findings indicate only a minor percentage of Aldrovanda
turions to overwinter successfully in the field (Kaminski, personal communication,
1994). This may be true for other aquatic carnivorous plant species. Therefore,
overwintering may be a critical phase of the growing cycle of aquatic
carnivorous plants. This has also been discovered by many carnivorous
plant growers. In orientation growth experiments in enclosures with intact
bottoms at natural sites in Poland, only 0-20% of the Aldrovanda
turions survived. In growth experiments in bottomless enclosures in the
Czech Republic, 0-70% of turions (on average, approximately 20-30%) survived.
Some turions in the Trebon region (S. Bohemia) hibernated on the top of
the wet bottoms and were grazed by small rodents. In the Doksy region
(N. Bohemia), turions were commonly grazed by ducks. Herbivores rarely
graze adult Aldrovanda but their grazing is focused on the energy-rich
turions. When turions overwintered below water at the same or similar
sites in the Trebon region, their survival was much higher (35-100%).
The rising of turions of aquatic carnivorous plants from the bottom is,
in some species, their most susceptible phase. Turion release from the
bottom is affected by how deep they are buried. In typical habitats of
aquatic carnivorous plants in shallow reed and sedge stands, the greatest
part of the litter, dead leaves and stems sinks to the bottom during the
winter and during elevated water levels in spring. The denser these emergent
stands, the more litter is available to bury the turions and impede their
rising. It also increases the anoxia at the bottom. Duckweed turions do
not germinate at O2 shortage. The same may be true for carnivorous
plant turions. Dense mats of filamentous algae or aquatic mosses may also
impede rising turions. Aldrovanda turions entangled on the boundary
between the bottom and free water may rot. However, turions of U. minor,
U. intermedia, and U. ochroleuca, which often grow in very
shallow waters, often germinate at the bottom.
Dense stands of reeds and sedges are not suitable habitats for summer
growth of aquatic carnivorous plants because of shading, nor are they
suitable for successful turion overwintering. The low overwintering rate
of Aldrovanda turions was observed after the wintering site had
been trodden underfoot by roe-deer. Afterwards, many of the turions germinated
as late as summer.
The paper is dedicated to my colleague Dr. Jan Kvet (Inst. Bot., Trebon,
Czech Republic) on the occasion of his 65th birthday and for his whole
life study of wetland plant ecology and great merits in wetland protection.
Adamec, L. 1995, Ecophysiological Study of the Aquatic
Carnivorous Plant Aldrovanda vesiculosa L., Acta Bot. Gall., 142:
Appenroth, K.J., Hertel, W., and Augsten, H. 1990, Photophysiology
of Turion Germination in Spirodela polyrhiza (L.) Schleiden, The
Cause of Germination Inhibition by Overcrowding, Biol. Plant., 32: 420-428.
Bartley, M.R., and Spence, D.H.N. 1987, Dormancy and
Propagation in Helophytes and Hydrophytes, Arch. Hydrobiol. (Beih.), 27:
Kaminski, R. 1987, Studies on the Ecology of Aldrovanda
vesiculosa L. II. Organic Substances, Physical and Biotic Factors
and the Growth and Development of A. vesiculosa, Ekol. Pol., 35:
Mazrimas, J.A. 1978, Aldrovanda, Carniv. Pl. Newslett.,
Newton, R.J., Shelton, D.R., Disharoon, S., and Duffey,
J.E. 1978, Turion Formation and Germination in Spirodela polyrhiza,
Am. J. Bot., 65: 421-428.
Winston, R.D., and Gorham, P.R. 1979a, Turions and Dormancy
States in Utricularia vulgaris, Can. J. Bot., 57: 2740-2749.
Winston, R.D., and Gorham, P.R. 1979b, Roles of Endogenous
and Exogenous Growth Regulators in Dormancy of Utricularia vulgaris,
Can. J. Bot., 57: 2750-2759.