E

Plant Div. Evol. Vol. 129/2, 125138

Published online February 2011

Microalgae trapped by carnivorous bladderworts

(Utricularia, Lentibulariaceae): analysis, attributes
and structure of the microalgae trapped
By Imad Aldeen Alkhalaf, Thomas Hbener and Stefan Porembski
With 8 figures and 3 tables

Abstract
Alkhalaf, I.A., Hbener, T. & Porembski, S.: Microalgae trapped by carnivorous bladderworts (Utricularia, Lentibulariaceae): analysis, attributes and structure of the microalgae trapped. Plant Div.
Evol. 129: 125138. 2011. ISSN 1869-6155.
Utricularia species capture small prey in traps. The prey spectrum of aquatic Utricularia species includes a large variety of organisms (e.g. copepods, cladocerans, crustacea, rotifers, algae). This study
focuses on selected attributes (species richness, density, biovolume, C and N contents) of microalgae
captured inside the traps of aquatic Utricularia spp.. A total of 850 traps of four aquatic bladderwort
species (Utricularia australis, U. foliosa, U. gibba and U. vulgaris) from tropical (Ivory Coast) and
temperate (Canada, Germany) regions has been investigated concerning the algae captured. In total,
302 microalgal taxa have been identified with Bacillariophyceae, Chlorophyceae and Charophyceae
being most species rich. The number of microalgae species captured was different among the Utricularia spp. It was relatively low inside the traps of U. gibba and U. foliosa from tropical Africa, with
the greatest species diversity observed within the Charophyceae (Desmidiaceae). The highest microalgae density, biovolume, C and N contents were observed within the traps of U. gibba/IC. There
are considerable differences in the amount and composition of algae trapped among the Utricularia
spiecies. The amount of microalgae captured does not relate to trap size parameters (length, height and
volume).
Keywords: Utricularia, bladderworts, microalgae, carnivory, nutrients, phytogeography.

Introduction
Carnivorous plants have developed numerous adaptations in order to attract, trap and
digest their prey (mainly insects) for obtaining essential nutrients such as nitrogen and
phosphorus (cf Barthlott et al. 2004). For certain carnivorous plants information on
prey spectra is available (e.g. Utricularia) but no comparative analyses exist with regard to the prey spectra between temperate and tropical regions.
Utricularia (Lentibulariaceae) comprises c. 220 species that are characterized by
their unique bladder traps (for a survey on their morphology see Taylor 1989). Trap
Received January 22, 2010, in revised form July 7, 2010, accepted July 9, 2010
2011 E. Schweizerbart
sche Verlagsbuchhandlung, Stuttgart, Germany

DOI: 10.1127/1869-6155/2011/0129-0037

www.schweizerbart.de

1869-6155/2011/0129-0037

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size usually ranges between 15 mm in length (Friday 1991) and most animals caught
(e.g. ciliates, crustaceans) are small. Depending on the size and type of trap, the size of
the captured prey animals can range from microscopic unicellular animals to vertebrates (Barthlott et al. 2007).
Remarkably, some aquatic species of Utricularia not only catch animal prey but
also have been observed to trap microalgae (e.g. Bacillariophyceae, Chlorophyceae)
with their suction traps. Recently (Mette et al. 2000, Daz-Olarte et al. 2007, Peroutka,
et al. 2008) the importance of the vegetarian diet of aquatic Utricularia species has
been investigated in more detail. It could be shown that in Germany a large number of
microalgae are trapped that might contribute to the nutritive supply (e.g. nitrogen) of
bladderworts (Alkhalaf et al. 2009).
Here we report for the first time on the results of analysis and attributes of the cyanobacteria and eukaryotic microalgae (in the following paper both labelled as microalgae or in case of multiple replication also algae) trapped by aquatic species of
Utricularia from differential geographical regions in order to get first insights about
possible region specific differences. Moreover, the C and N content of microalgae
captured by Utricularia traps was examined.

Material and methods

The following species of Utricularia have been studied:
Utricularia species

labelled as

locality of sampling

U. australis R. Br
U. vulgaris L.
U. vulgaris L.
U. foliosa L.
U. gibba L.

U. australis/GER
U. vulgaris/GER
U. vulgaris/CAN
U. foliosa/IC
U. gibba/IC

Retschow, Northeast Germany

Retschow, Northeast Germany
Rocky Mountains Region, Canada
Como National Park, Ivory Coast
Como National Park, Ivory Coast

All samples were taken between July 2006 and August 2007. The chemical characters of the waterbodies in northeast Germany are summarized in Table 1. Chlorophyceae is the most species-rich
group of the examinated Northgerman water-bodies and it was dominated by colony-forming species
such as Scenedesmus spp. Kirchneriella spp. Monoraphidium spp. and Dictyosphaerium spp.. The
Canadian lake is oligotrophic, acid and relatively shallow with a maximum depth of 2.5 m. U. folisa/
IC and U. gibba/IC were collected from a shallow, oligotrophic marsh. However, other chemical
properties of the tropical and Canadian lakes are not available in this paper.
The samples were preserved in 4% formalin solution for further inspection. In the laboratory, the
plants were divided into small segments with 23 traps per segment. A total of 850 traps was examined (U. australis/GER = 227 traps, U. foliosa/IC = 100 traps, U. gibba/IC = 100 traps, U. vulgaris/
CAN = 105 traps, and U. vulgaris/GER = 318 traps) to determine the microalgae captured. Microalgae adherent to the outer trap wall was removed by washing with distilled water.
The traps were cut and opened with a thin insect needle, the trap length was measured under a light
microscope as the greatest length from stalk end to trap-door end (Friday 1991) using the program
AnalySIS for windows. The traps were subdivided into eight size classes between 400 und 4200 m.
In order to calculate the volume the traps were divided into two parts (front as a cone, back as a half
sphere); the finally volume was calculated as the sum of both. The trap content was examined under a
light microscope (Zeiss Axioplan) and the microalgae or elements of them were subsequently deter-

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Table 1. Mean values of chemical variables measured between July 2006 and August 2007.
Kettle hole number
Mean parameter

K. 1

K. 2

K. 3

K. 4

Total-P (g L-1)
Orthophosphate (g L-1)
Total-N (g L-1)
NH4-N (g L-1)
NO3 (g L-1)
NO2-N (g L-1)
pH

0.18
0.08
3.38
0.17
0.08
0.005
6.6

0.08
0.02
4.21
0.12
0.11
0.005
7.1

0.42
0.05
6.97
0.19
0.66
0.009
6.5

0.06
0.02
1.46
0.08
0.03
0.004
6.7

mined and identified to the lowest taxonomic level possible. Algae biovolume was calculated for each
taxon using the formula for the geometric shape (Edler 1979, Reynolds & Bellinger 1992, Pohlmann
& Friedrich 2001, Vadrucci et al. 2007). The total algal biovolume was calculated by the addition of
the biovolume of all species present (abundance x volume).
Based on the total algal biovolume, carbon and nitrogen content of the various species of microalgae were determined using the conversion described by Menden-Deuer & Lessard (2000).

Results
Species composition
Microalgae assemblages in 850 traps of 4 aquatic Utricularia species were determined
(Fig. 1). In total, 302 taxa out of 82 genera belonging to 10 orders could be identified.
Most species rich were Bacillariophyceae (31% of the trapped algae, 21 genera, 95
taxa) and Chlorophyceae (31%, 35 genera, 94 taxa) followed by Charophyceae (Desmidiaceae) (28%, 13 genera, 84 taxa), cyanobacteria (7%, 10 genera, 21 taxa), Euglenophyceae (2%, 2 genera, 5 taxa) and Dinophyceae (1%, 1 genus, 3 taxa).
A relatively high number of microalgae was found in traps of U. vulgaris/GER (58
genera, dominant: Kirchneriella, Monoraphidium, Scenedesmus), 179 species. In traps
of U. australis/GER 58 genera/150 species were recorded. Dominant genera were Ankistrodesmus, Pediastrum and Scenedesmus. In traps of U. vulgaris/CAN 28 genera
(dominant: Cosmarium, Eunotia and Pinnularia) with at all 78 species have been
found. Lowest numbers were found in traps of U. foliosa/IC 24 genera/45 spp. (dominant: Cosmarium, Scenedesmus, Staurastrum) and U. gibba 11 genera/31 spp. (dominant: Closterium, Cosmarium, Staurastrum).
Concerning their relative abundance of all individuals, Chlorophyceae were dominant in traps of U. australis/GER (90%), U. vulgaris/GER (66%) and U. foliosa/IC
(41%). In traps of U. gibba/IC Desmidiaceae is dominant (83%) whereas in U. vulgaris/CAN-traps Bacillariophyceae such as Eunotia spp. is preponderant (58%).
Planktonic cyanobacteria, such as Microcystis spp., Chroococcus spp. were most

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Fig. 1. Species richness (total number of microalgae taxa found) in the traps of Utricularia spp.

Fig. 2. The percentage composition of the main algal groups recorded in the examined traps of four
species of Utricularia.

prominent in traps of U. vulgaris/GER (14%) and were completely absent from traps
of U. foliosa/IC and U. gibba/IC. Euglenophyceae were found in traps of all species
except U. vulgaris/CAN. Dinophyceae could only be recorded in traps of U. australis/
GER and U. vulgaris/GER.

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Density and biovolume of microalgae

There were obvious differences in the quantitative and qualitative composition of the
microalgae found in traps of the Utricularia species studied (Fig. 2, 3). The average
number of individuals per trap varied between the Utricularia species and ranged from
10 individuals per trap of U. vulgaris/CAN to 67 individuals per trap of U. australis/
GER. The value reached 48 individuals per trap of U. vulgaris/GER, 16 and 14 individuals per trap were by U. foliosa/IC and U. gibba/IC, respectively.

Fig. 3. Population density of captured microalgae in one mL trap volume.

Fig. 4. Total algae biovolume of the traps of Utricularia spp.

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Fig. 5. Biovolume percentage of microalgae taxa.

Algae density in the traps ranged from 2.5 103 cells mL-1 (U. vulgaris/CAN) to
92.8 103 cells mL-1 (U. gibba/IC). For details on all species studied see Fig. 3.
Total algae biovolumes ranged from 0.0236 mm3 mL-1 (U. vulgaris/GER) to 2.3 mm3
mL-1 in U. gibba/IC (Fig. 4). In Fig. 5 details are presented on the biovolume of individual groups of the microalgae. In general, Charophyceae and Chlorophyceae reach
the highest values. Euglenophyceae and Dinophyceae contributed a relatively minor
amount of biovolume.

Carbon and nitrogen content of microalgae

The capture of algae leads to an input of e.g. C and N into the traps of Utricularia depending on the quality and quantity of prey. The average total C and N that were potentially made available per trap differed widely between individual species of Utricularia (see Fig. 6). The C and N contents of captured algae in traps of U. gibba from
Ivory Coast were about four times higher than in the traps of U. vulgaris from both
Germany and Canada. The most interesting is that the both U. vulgaris/GER and U.
vulgaris/CAN have similar average values of C and N content per trap.
The Desmidiaceae contributed most C and N in the traps of U. foliosa/IC, U. gibba/
IC and U. vulgaris/CAN while Chlorophyceae were most important C and N contributors in traps of investigated Utricularia species in Germany (U. australis and U. vulgaris).

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131

Fig. 6. Mean contents (ng) of (A) carbon and (B) nitrogen of captured microalgae per trap.

Trap volume
The average volume of traps varied widely between individual traps of Utricularia
species. It was lowest in U. gibba/IC (0.15 0.08 mm3) and highest in U. vulgaris/
CAN (4 3.4 mm3) and U. foliosa/IC (4 1.1 mm3). The difference of traps volume
among the Utricularia species was significant (F = 78.3, p < 0.05).
The percentage ratio of total biovolume of microalgae captured/volume of traps
ranged between 0.002% and 0.23%. The highest value was recorded for U. gibba/IC
(0.23%) and the lowest value was 0.002% for both U. vulgaris from Canada and Germany. The percentage ratio reached a value of 0.009% and 0.003% for the other species from Ivory Coast (U. australis and U. foliosa), respectively (Fig. 7).

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Fig. 7. Relation between total volume of traps (mm3) and total biovolume of captured microalgae
(mm3).

Trap size and frequency of microalgae trapped

The length of Utricularia traps is generally larger than their height. The maximum
(4100 m) and minimum (460 m) values of the trap length were detected in U. vulgaris/GER. The height ranged between 143 m in U. australis/GER and 3700 m in
U. vulgaris/CAN (Table 2). The linear relationships between trap length and height are
correlated positively in the traps of all examined species.
In general, with the exception of U. vulgaris/GER, there was no significant relationship between trap size (length, height, volume) and the amount of microalgae captured.
The frequency distribution of the total number of captured algae varied with trap length
and height (Fig. 8) of the individual Utricularia species. In nearly all species of Utricularia, traps that captured the largest number of microalgae ranged from 0.7 to 8.0 mm3
in volume.

Table 2. Relation between the length (m) and height (m) of the examined traps.
Parameter

U. vulgaris/
CAN

U. foliosa/
IC

U. gibba/
IC

U. vulgaris/
GER

U. australis/
GER

Mean SD (L)
Max (L)
Min (L)
Mean SD (H)
Max (H)
Min (H)
p-value (L*H)
r2-value (L*H)

2286 570
4100
1358
1792 510
3700
1024
0.05
0.896

2335 241
2755
1257
2116 223
2581
950
0.05
0.707

852 146
1162
547
643 107
908
387
0.05
0.763

1975 706
3558
460
1636 528
3200
147
0.05
0.853

1668 472
2800
670
1387 439
2423
143
0.05
0.839

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133

Fig. 8. Frequency distributions of microalgae individuals across the (A) trap length (B) trap high and
(C) trap value.

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Discussion
The discussion focuses on the differences in microalgae spectra between the Utricularia species studied and on the amount of potential nutrients made available from the
microalgae trapped.
Species composition and microalgae spectra
The microalgae composition in the traps of Utricularia was similar to those described
in previous studies (Goebel 1891, Lemmermann 1914, Hegner 1926, Schumacher
1960, Mosto 1979, Wagner & Mshigeni 1986, Mette et al. 2000, Gordon & Pacheco
2007, Daz-Olarte et al. 2007, Peroutka et al. 2008, Sirov et al. 2009).
The differences in trapped microalgae diversity and composition might be a result
of differences in the general algae composition at the growth sites of the Utricularia
species studied (Zamora 1995) what could be due to particular physico-chemical features (Guisande et al. 2004, Peroutka et al. 2008). The qualitative and quantitative of
plankton composition is related to water temperature, light conditions, nutrient levels
and chemical changes (Fott 1971, Gordon & Pacheco 2007). Mette et al. (2000) showed
that aquatic bladderwort species in different German habitats do not capture their prey
objects selectively but in dependence on the available prey community and the prey
composition differs with regard to species and quantity.
It was also noted that only algae and not zooplankton were presented in the examined traps of Utricularia spp.. Gordon & Pacheco (2007) and Peroutka et al. (2008)
found that U. gibba and other aquatic Utricularia species contain more than 50% of
the examined traps algal taxa without zooplankton. Peroutka et al. (2008) further suggested that the number of trapped animals and algae did not correlate. The Euglena
spp. is trapped under controlled conditions without zooplankton presence (Jobson
et al. 2000).
Utricularia australis and U. vulgaris from Germany shared a considerable number
of trapped microalgae taxa (115) what is possibly due to the close neighbourhood of
the sampling sites. Eleven microalgae taxa (5 Bacillariophyceae, 4 Charophyceae, 2
Chlorophyceae) occurred in traps of both German and Canadian Utricularia species.
The microalgae spectra of U. foliosa and U. gibba from Ivory Coast differed considerably and only 6 taxa (out of 45 and 31 taxa recorded in traps of U. foliosa and U.
gibba, respectively) were in common (5 Charophyceae, 1 Euglenophyceae) what could
be the result of a larger distance between the sampling sites. Only very few microalgae
taxa (e.g. Pediastrum duplex, P. tetras, Ankistrodesmus gracilis) have been found in
traps of both temperate and tropical Utricularia species. Only one species (Cosmarium
laeve, Charophyceae) was observed in the traps of all species is examined. Some of the
identified algal taxa in the analyzed traps, like Ankistrodesmus falcatus, Dictyosphaerium pulchellum and Scenedesmus quadricauda, are cosmopolitan. They are found in
almost all water types and characterized by ubiquitous forms (Fott 1971).
This study as well as previous studies could not resolve the trapping process of the
microalgae and whether they are digested by Utricularia spp.. Mette et al. (2000) observed the algae trapped and found that they use the traps as a habitat in which they

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135

photosynthesize and reproduce. The traps may serve the algae as protection from predators (Wagner and Mshigeni, 1986). Desmidiales may favour the lower pH found inside the traps of Utricularia (Sirov et al. 2003, 2009) and Euglenphyceae may prefer
the trap environment due to high concentrations of organic nutrients (Palmer 1969).
Utricularia spp. possibly confine living organisms not only to absorb nitrogen and
phosphorous, also for the CO2 produced through respiratory activity of community
inside the traps (Gordon & Pacheco 2007).
We could not find a clear relationship between trap dimensions (length, height,
volume) and the amount of microalgae trapped what agrees with the results obtained
by other authors (Adamec 2009, Jobson & Morris 2001, Reifenrath et al. 2006, Sanabria-Aranda et al. 2006, Slack 2000). However, another important point is that the
amount of algae inside the examined traps of U. vulgaris/GER and U. australis/GER
showed significant relationships (p 0.05) to the pH, the conductivity as well as the
P- and N-concentrations of the water-bodies (data not shown). So our results do not
support the hypothesis of Peroutka et al. (2008) that no correlation among pH and
percentage of algae exists (Table 3).
Our results on trap size agree well with previous studies (Adamec 2009, Guiral &
Rougier 2007, Jobson & Morris 2001, Reifenrath et al. 2006, Sanabria-Aranda et al.
2006, Slack 2000, Taylor 1989). Friday (1991) calculated the mean volume values of
traps of U. vulgaris. They ranged from 0.11 to 8.45 L and from 1 to 4 mm in length.
These calculations are in agreement with our results. The trap size of Utricularia cf.
gibba from Brazil varied from 0.2 to 1.7 L in volume and from 0.7 to 1.5 mm in
length (Walker 2004).
The shape and size of Utricularia traps differ considerably between species and are
often used as an aid for species identification. Some species also show variation within
populations (Juniper et al. 1989). Guisande et al. (2000) suggested that the size and
number of the traps changing according to the prevailing conditions of the habitat. The
differences of trap size do not reflect differences in age of traps (Friday 1991) or stages in the growth of individual traps (Wallace 1975). In our Study, we found U. gibba/
IC has the smallest traps, but the amount of trapped algae in the traps was high. The
possible reason for this is that the abundance and quality of algae in their surrounding
water were higher than other habitats. The capture potential depends on the quality,
quantity or the availability of the organisms and on the environmental conditions in the
Table 3. Relation between the length, height and volume of the examined traps and the number of
microalgae individuals.

(L*n)

p-value
r2-value
(H*n) p-value
r2-value
(V*n) p-value
r2-value

U. vulgaris/
CAN

U. foliosa/
IC

U. gibba/
IC

U. vulgaris/
GER

U. australis/
GER

0.850
0.000
0.861
0.000
0.959
0.000

0.341
0.009
0.038
0.043
0.230
0.015

0.660
0.002
0.212
0.016
0.557
0.004

0.000
0.096
0.002
0.03
0.001
0.037

0.654
0.001
0.213
0.007
0.154
0.009

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habitats where the plants grow (Kurbatova & Yershov 2009, Zamora 1995). It is unquestionable that any variation on plankton communities will have an effect on prey
spectra (Zamora 1995). Gordon & Pacheco (2007) have shown that the prey composition reflects possibly the plankton biodiversity outside the traps.
Biovolume and C and N contents of microalgae
Differences in the biovolume of the microalgae trapped are due to different prey
spectra with U. gibba/IC ranking first (mainly trapping Charophyceae with relatively
large biovolume). Generally, the C and N contents of the microalgae trapped are comparatively low (maximum 39 and 8 ng C and N per trap). The total nitrogen content of
captured zooplankton inside the traps of U. australis/GER and U. vulgaris/GER ranged
from 105 to 346 ng N/trap and between 134 and 396 ng N/trap, respectively (own unpublished data) and is thus considerably higher.
The total nitrogen content of Utricularia tissue depends on its age (Friday &
Quarmby 1994). Tissue concentrations of N and P are usually below 2% and 0.1%,
respectively (Ellison, 2006). Carnivorous plants are able to extract 1087% of their
seasonal N content from animal prey (see Ellison & Gotelli 2001).
Moeller (1980) and Troxler & Richards (2009) have shown that tissue of U. purpurea is relatively rich in nitrogen (2.9% and 1.9% dry weight, respectively), but poor in
P (0.084% and 0.057%, respectively). Other aquatic species such as U. foliosa have a
N-content of 2.26% and the C:N ratio was 23 (Troxler & Richards 2009) with traps of
U. foliosa having a very high C:N ratio between 12 and 37 (Guisande et al. 2004).
Tissue contents of nutrients of U. australis senescent shoot segments depended significantly on the trophic level of habitats (Adamec 2008). The existence of microalgae
inside the examined traps does not imply that the captured algae is used as nutrition for
Utricularia. It is still not clear to what extent the nitrogen of the captured microalgae
is used by Utricularia.
The higher number of microalgae taxa in traps of temperate bladderworts could be
due to the higher number of traps examined from temperate Utricularia species. 45
algal genera were identified inside the traps of four aquatic Utricularia spp. from Austria (Peroutka et al. 2008). Sirov et al. (2009) have found more algal species inside the
traps of U. foliosa (126) and U. purpurea (132) from the Czech Republic.
Lewis (1978) reported that tropical lakes tend to have lower algae diversity than
temperate lakes. Kalff & Watson (1986) have found that the phytoplankton species of
tropical lakes do not, in large measure, differ from those in the temperate zone. The
differences in the taxonomic composition of the microalgae trapped by Utricularia
thus does not seem to be a function of latitude but seems to be rather the consequence
of stochastic events.
Acknowledgements
We thank Prof. Dr. W. Barthlott (Bonn), Prof Dr. D. Hessen (Oslo), Dr. P. Kosiba (Wroclaw), Dr. L.
Adamec (Tebo), Dr. R. Heerklo, Dr. D. Goetze, S. Adler (all Rostock) and N. Hobbhahn (Calgary)
for providing material and for valuable discussions.

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Addresses of the authors:
Imad Aldeen Alkhalaf, Thomas Hbener, Stefan Porembski, Universitt Rostock, Institut fr Biowissenschaften, Allgemeine und Spezielle Botanik, Wismarsche Str. 8, 18051 Rostock, Germany.
Corresponding author, e-mail: stefan.porembski@uni-rostock.de

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