DOI: 10.1007/s10967-007-1129-6 Journal of Radioanalytical and Nuclear Chemistry, Vol. 274, No.

2 (2007) 403409
02365731/USD 20.00 Akadmiai Kiad, Budapest
2007 Akadmiai Kiad, Budapest Springer, Dordrecht
Application of radiotracers in an exotic field of botany:
How to feed carnivorous plants
G. Steinhauser,
1
* W. Adlassnig,
2
M. Peroutka,
2
A. Musilek,
1
J. H. Sterba,
1
M. Bichler,
1
I. K. Lichtscheidl
2
1
Vienna University of Technology, Atominstitut der sterreichischen Universitten, Stadionallee 2, 1020 Vienna, Austria
2
University of Vienna, Cell Imaging and Ultrastructure Research Unit, Department of Cell Physiology and Scientific Film, Althanstr. 14,
1090 Vienna, Austria
(Received September 18, 2006)
In this paper, methods for the application of radiotracers in the Cobra Lily (Darlingtonia californica), a carnivorous pitcher plant, are described.
The uptake of radiotracers such as
42
K and
54
Mn into the pitcher trap in aqueous solution could be proven, whereas uptake of
59
Fe ions could not
be observed. No-carrier-added
54
Mn was taken up by the plants, regardless of extremely low concentrations. In contrast to earlier experiments
using
14
C and
15
N-based tracers, the methodology presented allows quick, simple and reliable quantification of the nutrient uptake. The results of
our experiments lead to a deeper biological understanding concerning the trace element household of this carnivorous plant and the absorption of
micro- and macronutrients from trapped prey.
Introduction
Plant nutrients
Carnivorous plants are specialized to live on
substrates with a low content of mineral nutrients. To
solve this problem, they developed the ability to catch
small animals in order to use them as additional nutrient
supply.
13
Since Justus von LIEBIG,
4
the main principles
of fertilizers and mineral nutrients for plants have been
known; the most important elements are nitrogen,
phosphorus, and potassium. Other essential elements are
sulphur, magnesium, calcium, sodium, boron,
manganese, iron, molybdenum, and many others.
5
Concerning carnivorous plants, most research so far
concentrated on the uptake of organic nitrogen
compounds from prey,
3,68
only little is known about the
uptake of other elements.
5,9,10
Focus was laid on plants
with adhesive traps.
1113
However, carnivorous plants
do not trap prey as a source of energy. It is assumed that
all species use the animals as a mineral nutrient supply.
The aim of this study was to develop a method for
the application of radiotracers to observe the uptake of
some essential micro- and macronutrients by pitcher
plants. For this study, potassium, iron, and carrier-free
manganese were chosen.
Potassium is the most frequent inorganic cation in
the cytoplasm. It influences the hydration of proteins.
14
Furthermore, it plays an important role in respiration,
chlorophyll development, photosynthesis, and it
contributes to the regulation of water content in the
leaves.
15
Potassium deficiency causes stunted growth, as
well as necrotic areas and chlorosis (yellow dis-
coloration of the leaves).
* E-mail: georg.steinhauser@ati.ac.at
Iron has a multifunctional role in the metabolism of
the plant.
15
Although iron is frequently taken up in the
ferric state (Fe
3+
), the ferrous state (Fe
2+
) is the most
common active form of iron in the plant. It is integrated
into cytochrome and into ferredoxin, which is necessary
for the light reaction in photosynthesis. Furthermore,
iron compounds are important for the electron transport
system in mitochondria. Iron is also needed for the
synthesis of chloroplast protein and it is a component of
various flavoproteins that are active in biological
oxidation. In the case of deficiency, extensive chlorosis
appears in the leaves.
The role of manganese in the metabolism of plants is
a topic of very recent biochemical and bioinorganic
research.
16
Manganese plays an important role as a
cofactor in photosynthesis, in particular in the
photosystem II, which uses light energy to oxidize water
to oxygen. This metalloradical mechanism uses a
tetranuclear manganese cluster and a tyrosyl
radical.
1722
Additionally, manganese is a cofactor in
superoxide dismutase. It is an essential element in
respiration and nitrogen metabolism.
Botanical background
Pitcher traps are a very diverse systematic group of
plants. 86 species from five families (Sarraceniaceae,
Nepenthaceae, Cephalotaceae, Bromeliaceae, and
Eriocaulaceae)
23
are known so far.
3,24,25
The species investigated in this study is the Cobra
Lily (Darlingtonia californica), which belongs to the
family of Sarraceniaceae (Fig. 1).
G. STEINHAUSER et al.: APPLICATION OF RADIOTRACERS IN AN EXOTIC FIELD OF BOTANY
404
Fig. 1. Darlingtonia californica; (a) artificial hole for pipetting tracer solutions; (b) entrance for prey insects
In general, pitcher plants contain aqueous fluid.
Trapped animals fall into this liquid and drown. Some of
the plants produce tensides in order to reduce surface
tension, which helps to prevent the escape of the trapped
animal.
27,26
Some of the plants have hairs which direct
the prey into the pitcher and make it even more difficult
to leave the trap. Most of the pitcher plants have a lid; it
does not close or move, but it has diverse functions like
chemical and visual attraction of prey or protection
against heavy rainfall.
The traps of Darlingtonia californica are an
exquisite example for the development of efficient prey
capturing. Animals are attracted towards the opening of
the pitchers by chemical attractants (nectar), by inwardly
oriented hairs, and by highly translucent areas in the
pitcher walls, which serve, in addition, to prevent
escape: animals that try to find the exit of the trap are
misled by the light coming through these areas. In
addition, downward pointing hairs impede their
climbing back up. They drown in a pool of digestive
fluid at the base of the pitcher and decay.
27,28
The digestion process in pitcher plants is performed
either by digestive enzymes produced by the plant itself,
mainly proteases, or with the help of microbes, feeding
on the decaying prey in the liquid.
2931
The plant
investigated in this study embarks on the latter strategy.
Experimental
General aspects
Radiotracers are an ideal tool for the observation of
nutrient uptake and metabolism of nutrients in biological
systems. To show whether carnivorous plants provide
themselves with potassium, iron, and manganese from
their prey, it might appear practicable to activate prey
insects, such as whole flies or ants, in the neutron flux of
a research reactor to produce radionuclides in the right
biological matrix. However, the authors did not embark
on this strategy for the following reasons:
(1) Denaturation of the proteins: The high neutron-
and -dose rates during activation and irradiation would
destroy the biological matrix within a very short time
and lead to the denaturation of the insects proteins. The
neutron flux in the central irradiation tube of the TRIGA
research reactor in Vienna is 1
.
10
13
s
1.
cm
2
, the -dose
rate inside the core of an operating reactor is extremely
high it is estimated to be approximately 10
7
Gy/h.
32
Additionally, the temperature inside the central
irradiation tube is approximately 343 K, leading to
further denaturation of biological tissues. Moreover, for
proper activation of iron, insects would have to be
irradiated for days and weeks to achieve an activity
sufficient for quantitative -detection. Insects treated this
way could not be compared with the natural prey.
G. STEINHAUSER et al.: APPLICATION OF RADIOTRACERS IN AN EXOTIC FIELD OF BOTANY
405
It must be suspected that the release of nutrients from
this drastically modified biological material is different
from the conditions in nature.
(2) Half-life of
56
Mn: Due to the short half-life of
56
Mn (T
1/2
=2.58 h), which is the direct (n,) activation
product of
55
Mn, the time of observation of the uptake
of manganese would be limited to only a few hours or 1
day at the very most. Digestion and uptake of nutrients
last a few days. Therefore, this strategy would
complicate a biological interpretation with regards to
manganese.
If living insects were activated by feeding with
radioactive food, an official permission, depending on
the country, would be needed. Moreover, such
experiments might raise ethical questions. Therefore, the
authors did not embark on this strategy either.
To solve these problems, aqueous solutions of the
respective ions were used. They simulate the natural
situation after decay of the insect and release of its
nutrients. Furthermore, the chosen elements are never
covalently bound in biological material, so the question
of possible digestion can be neglected. This
experimental design leads to comparable standardized
conditions for all tests, rather than applying activated
insects or insects fed with radioactive food, where
biological fluctuation (content of trace elements and
mass of the insect) would have to be considered.
Choice of the right anions
All nutrients investigated in this study were cations,
in particular K
+
, Fe
2+
, and Mn
2+
. The proper raw
material for the radiotracers has to be chosen carefully
and thoroughly. To show an example of a typical
problem: when irradiating a ferrous compound, for
example FeSO
4
.
7 H
2
O, Fe
2+
-ions are oxidized by the
immense rate of ionizing radiation in the operating
reactor (both, neutron- and -radiation).
The respective anion had to be chosen from the
following standpoints:
The chosen compounds must be easily soluble in
water. This is a very important demand to simulate prey.
Ions in the form of insoluble compounds are hardly
available to the plant.
The anion should not activate during irradiation in
the reactor in order to keep the plants - and -doses as
low as possible. Any unnecessary high irradiation of the
plants should be avoided in the experiments to minimize
stress symptoms due to cellular damage. Such
physiological stress would influence the uptake of
nutrients, because the epidermis cells performing
nutrient uptake proved to be very sensitive.
33
Furthermore, unnecessary irradiation should be avoided
to protect the researchers following the ALARA-
principle. Therefore, anions such as SO
4
2
, PO
4
3
, Cl

,
Br

, or I

should not be used.

The final solution of the radiotracers should be
weakly buffered and have a neutral pH-value in order to
avoid changes in the pH of the pitcher fluid, which
seems to be controlled in a quite complex manner in
Sarraceniaceae.
34
Therefore, the hydroxides, carbonates
and hydrogencarbonates were excluded. From the same
point of view, the researchers did not choose organic
anions, such as acetate or citrate: during irradiation,
organic compounds might decompose. The resulting
gases might burst the irradiation vials because of
overpressure inside the vial. Moreover, the metal ions of
a decomposed organic compound might form oxides.
Oxides are unusable for our radiotracer investigations,
because they either result in high pH-value of the
solution (potassium) or they have poor solubility and,
therefore, bioavailability (iron, manganese).
Keeping all these demands in mind, the authors
embarked on the following strategy. Potassium nitrate
was chosen as a raw material for all experiments with
potassium in this study. One could argue that plants
might take up nitrate and somewhat unintentionally
potassium ions, too, just to balance charges. However,
plants reach balance of charges by exudation of ions
with the same charge and not the uptake of ions with the
opponent charge. In case of the uptake of cations, H
3
O
+
ions are exuded preferably, a typical anion to be exuded
is succinate, if the plant takes up anions.
Uptake of iron and manganese was investigated
simultaneously. We activated metallic iron of high
purity to produce the desired radionuclides. After
irradiation with neutrons, the iron powder was dissolved
in hydrochloric acid. Thus, the compounds used for the
tracer investigations were FeCl
2
and MnCl
2
. In this case,
chloride concentrations were too low to disturb the
osmotic equilibrium of the plants.
Activation and preparation of the tracer solutions
For the observation of the uptake of potassium,
42
K
is a suitable radiotracer. For the stock solution
containing potassium, 43.79 mg KNO
3
were weighed
into a polyethylene vial and activated in the central
irradiation tube of the TRIGA Mark II reactor of the
Atominstitute in Vienna for 2 hours and 50 minutes. The
neutron flux density in this position is 1
.
10
13
cm
2.
s
1
.
After activation, the potassium nitrate was dissolved in
10 ml of distilled water, resulting in a concentration of
1.69 mg (activated) K
+
/ml. The resulting total
42
K-
activity was 35.35 MBq. Both, activity in the beginning
of the experiments and half-life of
42
K (T
1/2
=12.360 h),
are sufficient to trace the uptake of K
+
for up to five
days without problems.
For the preparation of the
54
Mn and
59
Fe containing
stock solution, 87.55 mg of iron powder (E. Merck,
Darmstadt, pro analysi) were irradiated for 15 days in a
Suprasil quartz glass vial covered with a cadmium
G. STEINHAUSER et al.: APPLICATION OF RADIOTRACERS IN AN EXOTIC FIELD OF BOTANY
406
envelope in the reflector irradiation tube of the TRIGA
reactor in Vienna. Both radionuclides are generated from
iron by the nuclear reactions
58
Fe(n,)
59
Fe and
54
Fe(n,p)
54
Mn. The cross section for the latter reaction
is 63 mb for irradiation with fast reactor neutrons.
35
With this method, carrier-free manganese is produced, in
this particular case 3
.
10
15
mol. The fast reactor neutron
flux density is 1.4
.
10
10
cm
2.
s
1
in this irradiation
position, yielding activities of
59
Fe and
54
Mn of 660 and
4690 Bq, respectively. The half-lives of
59
Fe and
54
Mn
are 44.495 days and 312.12 days, respectively. After
irradiation, the iron powder was dissolved in
hydrochloric acid (Riedel-de Han, min. 37%, R.G.)
under oxygen-free conditions and heated carefully. The
excess of hydrochloric acid was removed by partially
evaporating the solution. During evaporation, 12.5 mg
inactive iron powder were added and dissolved to ensure
the ferrous state of the solution by the following
comproportionation reaction:
2Fe
3+
+ Fe
0
3 Fe
2+
The resulting solution was diluted to obtain two
stock solutions with concentrations of 0.1 and 1 mg
Fe
2+
/ml. In addition, ascorbic acid was added to the
solution in both cases in a concentration of 0.3 mg/ml to
decelerate oxidation of Fe
2+
. This amount of ascorbic
acid can be regarded as harmless for plants.
36
For this
test series, no inactive manganese carrier was added.
A summary of the stock solutions, their
concentrations, activities, and the respective aliquots can
be found in Table 1.
Administration of the radiotracers
Radiotracers were administered by pipetting an
aliquot of the stock solution into the plants pitcher,
which is mechanically troublesome in case of
Darlingtonia californica, because the pitchers entrance
is on the bottom side of the leave. Therefore, an artificial
hole had to be cut into the plants tube to allow for
secure pipetting (Fig. 1). The amount of nutrients was
chosen by comparison with typical insects contents of
the respective nutrients. A bluebottle fly (Calliphora
erythrocephala) contains approximately 70 g
potassium. Since the typical prey of Darlingtonia
californica is somewhat smaller, the aliquot for
experiments with potassium was only approximately
half of this amount, namely 33.8 g K
+
. The insects
typical content of iron is approximately 10 g.
37
To
cover a wider range, in the case of iron this amount was
administered, as well as an aliquot one order of
magnitude above the minimum nutrient package.
After a certain time span of 1, 24, 48 hours in the
case of potassium experiments and 24, 48, 168 hours in
case of Mn/Fe experiments, the treated pitchers were cut
off and washed thoroughly three times with 10 ml of
washing solution. It contained the same ions as the
tracer solution in order to better rinse active ions from
the interior surface of the pitcher, which may have been
adsorbed without any uptake by the plant. The
concentration of the respective cation in the washing
solution was about the same as it was in the pitcher.
After the last step of washing, the washing water was
tested to be almost inactive.
To check the adsorption of radiotracer ions on the
inner surface of the pitcher, the following control was
performed. An aliquot of 100 g Fe
2+
(containing
54
Mn
2+
, too) and an aliquot of 33.8 g K
+
were pipetted
into selected pitchers. After 60 seconds, the pitchers
were cut off, washed as described above, and measured
using a -detector. Adsorption on the inner surface of the
pitcher was found to be almost negligible.
Detection
Gamma-measurement and quantification of the
amount of radiotracers taken up by the plants was
performed using a 151 cm
3
HPGe-detector (1.8 keV
resolution at the 1332 keV
60
Co peak; 50.1% relative
efficiency), connected to a PC-based multi-channel
analyzer with preloaded filter and Loss-Free Counting
system.
38,39
Quantification was performed by
comparison of the peak areas of the respective
radionuclides contained in plant and stock solution in
the same geometry on top or beside the detector. To
obtain a comparable geometry, plants were pressed into
a vial. Measurement lasted for 4700 seconds in case of
experiments with potassium and 1 day in case of iron
and manganese.
For quantification, the following -lines were
chosen:
42
K 1524.6 keV (18.08% -efficiency)
54
Mn 834.848 keV (99.9760% -efficiency)
59
Fe 1099.245 keV (56.5% -efficiency)
Table 1. Summary of concentrations and activities of stock solutions and aliquots used for the experiments investigating nutrient uptake
Stock Solution Aliquot
Concentration Activity Volume, l Ion content Activity
1.69 mg K
+
/ml 3.54 MBq/ml (
42
K) 20 33.8 g K
+
71 kBq
42
K
100 g Fe
2+
/ml 0.7 Bq/ml (
59
Fe); 4.7 Bq/ml (
54
Mn) 100 10 g Fe
2+
; 1.6 fg Mn
2+
0.07 Bq
59
Fe; 0.47 Bq
54
Mn
1 mg Fe
2+
/ml 6.6 Bq/ml (
59
Fe); 46.9 Bq/ml (
54
Mn) 100 100 g Fe
2+
; 16.4 fg Mn
2+
0.7 Bq
59
Fe; 4.7 Bq
54
Mn
G. STEINHAUSER et al.: APPLICATION OF RADIOTRACERS IN AN EXOTIC FIELD OF BOTANY
407
All nuclear data in this paper were taken from the
National Nuclear Data Center,
40
Brookhaven National
Laboratory, unless otherwise noted.
Results and discussion
The method described in this paper offers the
possibility to observe the uptake of metallo-nutrients
from prey insects by carnivorous plants. Experimental
results are listed in Table 2 and Fig. 2, showing that
potassium and manganese are taken up by the plant to a
quite high extent (up to 88% in case of K
+
and up to
41% in case of Mn
2+
), iron is not taken up in detectable
amounts.
Darlingtonia californica takes up potassium very
quickly. Less than 2% of potassium is adsorbed within
60 seconds on the inner surface of the plants pitcher.
Therefore, uncertainties in the same order of magnitude
for the K
+
-results presented should be taken into
account, additionally to the errors due to counting
statistics. Only one hour after feeding, 19% of potassium
have been taken up. After at least 24 hours,
incorporation reaches a plateau between 85 and 90%,
where no more potassium is absorbed, as shown in
Fig. 2.
Table 2. Uptake of potassium and manganese in a certain time after pipetting the aliquot
into the pitcher
Uptake
Radioisotope Duration
Absolute Relative, %
Error, %
33.8 g
42
K 60 s 0.667 g 2.0 4
1 h 6.44 g 19.1 2
24 h 29.7 g 87.9 2
48 h 29.4 g 86.9 4

1.6 fg
54
Mn 24 h n.d.
48 h 0.26 fg 16 >10
168 h 0.67 fg 41 >10

16.4 fg
54
Mn 60 s n.d.
24 h 0.64 fg 3.9 6
48 h 0.61 fg 3.7 >10
168 h 2.95 fg 18 9
Relative uptake in percent of the administered amount (given in the first column) of the
respective nutrient. Errors due to counting statistics.
n.d.: Not determined.
Fig. 2. Uptake of K
+
and Mn
2+
as percentage of the administered aliquot after a certain time
G. STEINHAUSER et al.: APPLICATION OF RADIOTRACERS IN AN EXOTIC FIELD OF BOTANY
408
In contrast, the uptake of iron could not be observed
in detectable amounts. The detection limit for iron in
these experiments was 3 g. It has to be taken into
account that Fe
2+
might have been oxidized to Fe
3+
by
atmospheric oxygen, regardless of the addition of
ascorbic acid. Ferric compounds are less available for
plants. However, in spite of the very low concentration
of all nutrients, virtually all iron is bioavailable in peat
soils.
41
So we assume that Darlingtonia does not depend
on iron supply from its prey as it does in the cases of
potassium and manganese.
Carrier-free manganese is taken up by the
carnivorous plants of this study, regardless of extremely
low concentrations. This implies that the plants
mechanism for the uptake of nutrients is extremely
selective with manganese, even in an iron-rich matrix.
However, higher concentrations of iron partly impede
the uptake of manganese (Fig. 2). This might also be due
to the good availability of iron in peat soils: manganese
deficiency is caused not only by little manganese in soil,
but also by a critically low Mn: Fe ratio.
42
If well
supplied with iron, Darlingtonia, therefore, develops an
additional need for manganese.
Former studies on uptake of elements applied
methods like micro-autoradiography with, e.g.,
14
C-
labeled proteins, amino acids or sugars, or non-
radioactive
15
N-compounds were used.
4346
Auto-
radiography-techniques display mainly the dispersal of
macronutrients in the plant but hardly offer
quantification. In contrast, the newly developed method
presented here, provides quick and reliable quantitative
data on the uptake. The detection limits are low, and
thus uptake of even small amounts of substances can be
observed. This advantage qualifies our method not only
for the investigation of macronutrient uptake, but also
for experiments with micronutrients, where non-
radioactive tracers cannot be applied without high
analytical effort.
Conclusions
The uptake of potassium and manganese from
(simulated) prey by the carnivorous pitcher plant
Darlingtonia californica (Sarraceniaceae) could be
proven, whereas no uptake of iron could be observed.
This is the first direct evidence for the uptake of
potassium and manganese from prey by carnivorous
plants. The application of radiotracers could provide a
first insight into the trace element and nutrient
household of this plant, which is still an exotic and
barely understood field of botany. Further investigations
will comprise other carnivorous pitcher plants, such
as Cephalotus (Cephalotaceae) or Heliamphora
(Sarraceniaceae). Additionally to the methods presented
in this paper, the authors will use a manganese carrier to
study the uptake of higher concentrations of manganese,
which becomes poisonous for plants after a narrow
range of essentiality. Furthermore, the uptake of Fe
2+
and Mn
2+
-complexes, such as EDTA complexes, by
carnivorous plants will be investigated. These
complexes, which are more stable against oxidation,
simulate preys protein-bound iron and manganese.
*
This study was supported by Grant H-2187/2006 of the
Hochschuljubilumsstiftung der Stadt Wien. The authors wish to thank
the members of the reactor group of the Atominstitut (in particular M.
VILLA, E. KLAPFER, and H. SCHACHNER) for the good co-operation.
Moreover, thanks are due to R. WESSELY and his team, in particular
M. EDLINGER from the Bundesgrten Schnbrunn, who took care of
the plants, and T. LENDL for his support with literature and plants.
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