Plant Ecol (2008) 199:153–162 DOI 10.1007/s11258-008-9420-3
Utricularia: a vegetarian carnivorous plant? Algae as prey of bladderwort in oligotrophic bogs Marianne Peroutka Æ Wolfram Adlassnig Æ Michael Volgger Æ Thomas Lendl Æ Walter G. Url Æ Irene K. Lichtscheidl
Received: 9 October 2007 / Accepted: 14 March 2008 / Published online: 8 April 2008 Springer Science+Business Media B.V. 2008
Abstract Aquatic carnivorous plants of the genus Utricularia capture and utilise a wide range of small aquatic organisms. Most of the literature focuses on animals as prey. In this study, we investigate the occurrence of algae inside the traps of four species of bladderwort. We observed that algae of 45 genera form up to 80% of the total prey; algae were found frequently in traps without animal prey. The majority are coccal and trichal algae of the families Desmidiaceae and Zygnemataceae. The percentage of algae increases significantly with decreasing electric conductivity of the water (rS = -0.417; P = 0,000). Thus, algae are the most frequent prey in extremely soft waters. The percentage of algae did not differ significantly, not within the investigated Utricularia species or within the various study sites. However, the taxonomic composition of the algal prey showed highly significant differences between different sites. More than 90% of the trapped algae were killed and degraded by the bladders. The recent data allow for two alternative hypotheses: either algal prey
M. Peroutka (&) W. Adlassnig M. Volgger T. Lendl I. K. Lichtscheidl Cell Imaging and Ultrastructure Research, Department of Cell Physiology and Scientific Film, The University of Vienna, Althanstrasse 14, 1090 Vienna, Austria e-mail:
[email protected] W. G. Url Museum of Natural History, Burgring 7, A-1010 Vienna, Austria
supplements animal prey in oligotrophic waters, or the unprofitable trapping of algae is rather an additional stress factor for Utricularia and contributes to its limited distribution in some peat bogs. Keywords Carnivorous plant Desmidiaceae Mineral nutrition Prey selection Water chemistry Zygnemataceae
Introduction Evolutionarily, Utricularia is the most derived genus of the carnivorous family Lentibulariceae. So far, 220 species have been described (Barthlott et al. 2004), of which about 25% are aquatic (Taylor 1994). All species are equipped with highly sophisticated suction traps which produce a negative hydrostatic pressure in a hollow bladder. In most species, the stimulation of sensitive hairs by tiny animals triggers a rapid influx of water which carries the prey into the trap (Guisande et al. 2007; Juniper et al. 1989; Sydenham and Findlay 1973). Inside, the prey dies from anoxia (Adamec 1995, 2007) and is dissolved by digestive enzymes produced by glandular hairs that line the inner side of the trap (Vintejoux 1973, 1974; Vintejoux and Shoar-Ghafari 2005). In some species, the supply with organic compounds from prey was shown to be essential for vigorous growth and reproduction (Pringsheim and Pringsheim 1967).
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However, even after 130 years of research, the trapping mechanism is not yet fully understood (Darwin 1875; Juniper et al. 1989; Lloyd 1942; Sydenham and Findlay 1973; Sydenham and Findlay 1975; Tschumpel 2002). In aquatic species, most of the animal prey consists of crustaceans; furthermore, insects, rotifers, nematodes, acari and protozoa are found frequently (Barthlott at al. 2004; Cohn 1875; Darwin 1875; Garbini 1898 cited after Hegi 1906; Harms 1999; Harms 2002; Hegner 1926; Mette et al. 2000; Seine et al. 2002). Non-animal prey was considered only by few authors. Cohn (1875) was the first to observe algae trapped in the bladders. The author thought that the algae had originally grown epizoic on trapped animals and propagated in the nutrient rich environment of the trap. Botta (1976), Darwin (1875), Hegner (1926) and Schumacher (1960) found similar results and described communities of living and propagating algae inside the traps. They detected mainly Cyanophyta, Bacillariophyta, Chrysophyta, Euglenophyta and Chlorophyta. The same taxa were found by Gordon and Pacheco (2007) who worked with fixed samples. The most common taxa within Chlorophyta were various genera of Desmidiaceae (Schumacher 1960). From these observations, the hypothesis arose that algae would live as symbionts in the trap of Utricularia L. which might benefit from carbohydrates produced by the algae. Mette et al. (2000) found twelve taxa of algae (six Chlorophyta, two Euglenopyhta, three Dinophyta and one Bacillariophyte) inside the traps of Utricularia vulgaris L., U. australis BROWN and U. macrorhiza LE CONTE. These algae were killed and digested like animal prey. Tschumpel (2002) found similar results: algal prey was degraded in vivid traps, whereas living communities were only formed in old inactive bladders. Jobson et al. (2000) used Euglena sp. in a series of feeding experiments. Utricularia uliginosa VAHL trapped and digested huge amounts of Euglena, but showed reduced growth compared to the unfed control. These results indicate that exclusive algal prey provides insufficient nutrient supply. Feeding with both algae and metazoa, however, led to a strong increase in biomass. In this study, we tested the following hypotheses: •
A significant amount of Utricularia prey consists of algae.
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•
•
•
•
The percentage of algae and animals inside the traps depends on the aquatic environment of the Utricularia plant. Algae are not only trapped together with animals, but are sucked into the bladders without animal prey triggering the trap. Algae are not surviving and propagating inside active bladders, but are killed and degraded like other prey; thus, the ‘‘symbiosis hypothesis’’ is wrong. Specific taxonomic groups as well as growth forms occur among the prey of Utricularia.
Methods Plant material and study sites We analysed the prey of four species of Utricularia, i.e. U. vulgaris L., U. australis BROWN, U. minor L. and U. bremii SCHULZ (fide Adler et al. 1994; Aeschimann et al. 2004; Hegi 1906; Taylor 1994; Thor 1988). The plants were collected in Austria in six different mires, each consisting of several hollows in the provinces of Lower Austria, Tyrol and Vorarlberg, one artificial pond and one anabranch of the river Danube in Vienna. All samples were taken in late summer from 2001 to 2005. In two sites plants were sampled twice: in Sulzberg (2001 and 2005) and Schwarzes Moos (2002 and 2004). Details on the experimental sites are given in Table 1. Specimens of all collected populations are preserved in the herbarium of the authors. Sampling and analysis of the trap content In all habitats, we determined pH and conductivity of the water, using a WTW Microprocessor pH-meter 320 and a Pure Water Tester LT-Lutron WA-300. Most investigated water sites were shallow hollows or ponds with a depth of only a few centimetres. In deeper water bodies, the plants were swimming at the water surface. Since all plants were constantly exposed to water movements due to wind and rain, no specific precautions were taken to protect the traps against mechanical irritations during transport. The plants were collected in glasses with ambient water. The containers were kept open, under indirect light
176 m
E 16 32.1460
N 48 12.0250
Vienna
222 m
E 16 21.5810
N 48 13.6760
Vienna
709 m
E 11 33.0780
N 47 18.3430
Tyrol, Baumkirchen
926 m
E 10 02.2190
N 47 24.4840
Vorarlberg, Sibratsgfa¨ll
988 m
E 09 53.5990
N 47 30.5590
Vorarlberg, Sulzberg
954 m
E 09 54.1610
N 47 31.1810
Vorarlberg, Sulzberg
593 m
E 15 08.7370
N 48 51.2630
Lower Austria, Gemeindeau
510 m
E 14 58.7430
Source of detailed information
Anabranch
Artificial pond
Calcareous minerotrophic fen
Calcareous-mesotrophic percolation fen
Subneutral-mesotrophic percolation fen
Subneutral-mesotrophic percolation fen
Channel between a fish pond and an acid-oligotrophic aggredation fen
Schratt 1988
Grabherr and Polatschek 1986; Repitz 1993; Schreiber 1910; Steiner 1992
Grabherr and Polatschek 1986; Repitz 1993; Steiner 1992
Repitz 1993; Steiner 1992
Adlassnig et al. 2005; Pranjic´ 2004; Steiner 1985; Steiner 1992
Ombrogenic, acid-mesotrophic Pranjic´ 2004; Pranjic´ et al. 2006; fen with many peat bogs Steiner 1985; Steiner 1992
Hydrological type
The names and classification of the mires are taken from Grabherr and Polatschek (1986) and Steiner (1992)
Lobau
Postteich
Baumkirchner Tal
Moor am Kra¨henberg
Niedermoor su¨dlich Ko¨hlerweg
Moos 1
Gemeindeau
Lower Austria, Brand-Nagelberg
Schwarzes Moos
N 48 52.345
Position
Site
Table 1 Description of the sampled sites
1
1
1
1
2
5
1
3
Number of investigated water sites
U. vulgaris
U. australis
U. minor
U. bremii
U. minor
U. minor
U. australis
U. australis
Utricularia species
206
109
50
115
139
430
69
332
Number of traps investigated
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and protected against extreme temperatures. Under these conditions, algae from peat bogs usually stay alive for several months (Lenzenweger 1996). The bladders and their prey were analysed within 6–48 h after collection. We examined only fully grown but vivid traps that were formed by water shoots. Colourless subsoil shoots (‘‘Schlammsprosse’’, Hegi 1906) of some species were excluded, since they were not accessible to algae. In earlier studies, traps for the analysis of prey were chosen irreproducible (Jobson et al. 2000; Mette et al. 2000) or at random (Harms 1999). For the present study, a random approach was not applicable because algae can be expected to propagate in old, inactive traps. Therefore, we observed only traps within the youngest parts of the shoot. The youngest traps next to the bud were still immature and therefore excluded. Observation started with the first trap containing prey and continued for 20 cm maximum, unless indications of senescence were found before. On average, six to twelve traps per shoot were analysed. We quantified the content of 1,450 traps. We distinguished between animals, various taxa of algae, protozoa and detritus. Multicellular algae, like colonies or filaments, were counted as one individual each. Detritus particles, Sphagnum leaflets, etc. were rated as prey items as well. Due to the heavy decomposition of the prey, determination was only possible to the generic level in most cases. In order to avoid contamination by epiphytic algae and animals, the traps were not sliced, but analysed in the intact state using long distance objective lenses. Sporadic traps with pigmented, opaque walls were excluded. Vitality of algae proved to be difficult to evaluate in intact traps. Therefore, the percentage of dead and living algae were determined in 25 traps of Utricularia minor from Moor 1 at Sulzberg. These traps were washed thoroughly in order to remove adhered algae and cut open. Cells were counted as dead when the protoplast of the algae showed any damage, when chloroplasts were contracted (Bancher and Ho¨fler 1959) or when the cytoplasm absorbed 1% Cyanol (Blinks 1942). Statistic treatment The Kolmogorov–Smirnov Test gave evidence that none of our samples showed Gaussian distribution (P \ 0.000). Transformation to lognormal
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distribution proved to be not applicable because of numerous traps without any prey. Thus, we used the non-parametric Mann–Whitney U-Test to compare the percentage of algae in traps of the different Utricularia species, sampling sites and geographic regions. Correlation between the percentage of algae and water parameters was tested by Spearman Rank Correlation for non-Gaussian distribution of data. All tests were performed for standard significance levels of a = 0.01 and a = 0.001. All statistic analyses were performed using SPSS 10.0.
Results Composition of the trap content and water chemistry We analysed 1,450 traps of four Utricularia species from eight sites with fifteen water bodies. Altogether, 1,219 of these traps contained some visible trap content; in 825 traps algae could be detected (Fig. 1). Electrical conductivity and pH of the water as well as the composition of the trap content are given in Table 2. The quantitative composition of the prey strongly depended on the habitat: in mesotrophic ponds with hard water, only few algae were found, whereas in oligotrophic peat bogs with soft water, algae formed the great majority of the trap content (Fig. 2). The conductivity of the water and the mean percentage of algae in the total prey of each site were highly significantly correlated (rS = -0.417; P = 0,000; Fig. 2). We also compared all traps from soft (conductivity lower than 150 lS cm-1) with rather hard or eutrophic waters (conductivity higher than 150 lS cm-1). In soft waters, an average trap contained 4.8 algae (i.e. 75.0% of the total prey), in eutrophic waters only 1.8 (i.e. 21.1%). The difference was significant on a level of a = 0.001. In extremely soft water, Utricularia was very rare. In Moos 1, e.g. it was found in only one of seven hollows with a conductivity lower than 20 lS cm-1. In Schwarzes Moos, on the other hand, Utricularia colonises all ponds with a conductivity of higher than 40 lS cm-1. Clear evidence was found that the number of trapped animals and algae did not correlate (rS = 0.138; P B 0.0005). Furthermore, there is no
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was Cosmarium spp. (Desmidiaceae). Furthermore, Cyanobacteria [especially Anabaena spp. (Nostocaceae)] and various Chlorophyta [especially Eremosphaera viridis (Oocystaceae)] were commonly found. All other groups of algae were very rare, even the common Bacillariophyta (Table 5). All these taxa are common in the waters inhabited by Utricularia, especially in the epiphyton of the Utricularia plants. Accordingly, we found differences in the composition of algae between various geographical regions. In the oceanic mires of Vorarlberg, Desmidiaceae were dominant. In the subcontinental fens in Lower Austria, Mougeotia (Zygnemataceae) and other filamentous species dominated among the prey as well as in the surrounding waters. In Lobau and Postteich, Cladophora sp. (Cladophoraceae) was dominant in the periphyton, but not trapped by Utricularia. Other trap content besides algae
Fig. 1 Micrograph (A) and line drawing (B) of a typical Utricularia minor bladder from a soft water fen habitat (Moos 1). Ten algae, i.e. four Eremosphaera viridis (a), one Closterium sp. (b), one filament of Desmidium swartzii (c), one Pleurotaenium trabaeculae (d), two Pleurotaenium spp. (e) and one Euastrum humerosum (f), are clearly visible in the intact bladder. Only two remnants of animals—carapaces of microcrustaceans (g) —can be recognized. Some detritus (h) cannot be identified
obvious correlation between pH and percentage of algae. Differences in prey composition between the four tested species of Utricularia were not significant. We identified 45 genera of algae trapped in Utricularia bladders (Table 3). In all sites, more than 95% of all individuals belonged either to the coccal or to the trichal growth form. Occasionally we also found capsal and monadal algae (Table 4). Siphonal and siphonocladal forms were lacking completely, as well as branched filaments. Taxonomically, more than 70% of the trapped algae belonged to the Zygnematophyta, at all sites. Of all algae, 28.2% (i.e. 20.0% of all identifiable prey)
Animals formed the second largest group of prey organisms. We observed mainly microcrustaceans but also acari, nematodes and insect larvae. Of the trapped animals, 14.3% (i.e. 3.2% of all identifiable prey objects) were protozoans, many of them still alive. Mucilaginous colonies of bacteria were found sporadically. In Baumkirchner Tal, where at average only 1.49 prey objects were found per trap, bacterial colonies formed 12.1% of the total trap content. In all other sites, the percentage of bacteria was negligible. Occasionally, the trap content was also composed of pollen grains, fungal spores, Sphagnum leaflets and unidentifiable detritus. In one hollow of Moos 1, a weak correlation between the number of algae and detritus particles was observed (rS = 0.300, P = 0,000). In all other study sites, no such correlation occurred. Altogether, no significant correlation between the number of trapped algae and detritus could be found as well (rS = 0.093; P = 0000). Algae are degraded within the trap We analysed the living status of the prey from 25 traps from Moos 1 containing 100 algal objects with altogether 575 cells. Of these, 93 algae (93%) with a total of 565 cells (98.3%) were dead. In many traps, the protoplast of the prey algae was damaged and
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Table 2 Comparison of the water parameters and the trap content from the test sites Percentage of Percentage of Percentage of Number of traps with traps with traps with traps with prey (%) algae only animals both algae (%) only (%) and animals (%)
Number of trapped genera of algae
47–96
93.4
21.7
14.2
56.3
24
360 14–62
53.6 71.9
2.9 46.3
29.0 1.4
10.1 20.5
5 21
84.2
26.6
3.6
48.9
17
82.6
19.1
15.7
31.3
7
84.0
30.0
14.0
34.0
11
78.9
8.3
38.5
22.9
8
79.1
23.3
16.5
29.1
2
Site
Range of pH
Range of conductivity (lS cm-1)
Schwarzes Moos
4.4–4.8
Gemeindeau Moos 1
6.0 5.5–7.2
Niedermoor su¨dlich Ko¨hlerweg Moor am Kra¨henberg
7.0–7.6
104–140
6.8
424
Baumkirchner Tal Postteich
7.5
Lobau
7.6
324
Traps with detritus only are not included. Traps containing only unidentifiable remnants or debris are not included
Discussion Algae are trapped by Utricularia
Fig. 2 Relation between the conductivity of the water and the percentage of trapped algae in the prey. Each dot indicates the mean value for one sampling site. The curved lines indicate the 0.99 confidence interval (rS = -0.417; P = 0.000). The grey bar indicates extreme soft waters where Utricularia was not found
often lacking completely. Only 7% of the algae were alive. A similar result could be found in the screening of the other 1,425 Utricularia traps within the first 20 cm below the shoot apex, where most trapped algae were apparently dead. Communities of definitely living algae were frequently found in old, obviously inactive or dead traps, but those were not quantified in the present study. Algae outside the traps or attached to the Utricularia plants were alive. Filamentous algae were found frequently ensnarled with the bristles of the traps as well as with other parts of the plant.
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We found 45 genera of algae as prey organisms, belonging to diverse growth forms and systematic groups. Large thalli were missing which is explained by the small size of the bladder. Experiments under controlled conditions showed that even unicellular algae far too small to stimulate the bristles of the bladder can be trapped (Jobson et al. 2000). In the natural habitat, the dominant prey species move by gliding (e.g. Oscillatoria, many Desmidiaceae), or they float between the plants without being attached (e.g. Anabaena, Zygnemataceae). Epiphytic species (Gloeotrichia, Characiopsis, Tribonema, Oedogonium) were commonly found in the periphyton, but less frequent as prey objects. Planktonic (Asterionella, Tabellaria) and actively swimming species (mainly Peridinium or Phacus, both also mentioned by Mette et al. 2000) occurred only occasionally. Euglena, which is trapped frequently by U. uliginosa (e.g. Hegner 1926; Jobson et al. 2000; Sirova et al. 2003), was very rare as well. This special case may be due to the low abundance of Euglena in undisturbed fen waters of the Austrian Alps (Loub et al. 1954). Among the animal prey, a similar preference for climbing species is known from the literature (Harms 1999). The prey spectrum shows that the mechanism of the trap is not efficient enough to tear off epiphytes. Furthermore, the water flow is too small to enrich significant amounts of planktonic organisms. Only
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Table 3 Genera of algae found in Utricularia traps Anabaena (Nostocaceae)
Fragilaria (Fragilariaceae)
Pinnularia (Naviculaceae)
Asterionella (Fragilariaceae)
Gloeotrichia (Rivularaceae)
Pleurotaenium (Desmidiaceae)
Chara (Characeae; spores only)
Gymnozyga (Desmidiaceae)
Rhizoclonium (Cladophoraceae)
Characiopsis (Characiopsidaceae)
Hyalotheca (Desmidiaceae)
Spirogyra (Zygnemataceae)
Chlamydomonas (Chlamydomonadaceae)
Melosira (Coscinodiscaceae)
Staurastrum (Desmidiaceae)
Chlorella (Oocystaceae)
Micrasterias (Desmidiaceae)
Staurodesmus (Desmidiaceae)
Chroococcus (Chroococcaceae)
Microcystis (Chroococcaceae)
Surirella (Surirellaceae)
Closterium (Desmidiaceae)
Microspora (Microsporaceae)
Tabellaria (Fragilariaceae)
Cosmarium (Desmidiaceae)
Mougeotia (Zygnemataceae)
Tetmemorus (Desmidiaceae)
Desmidium (Desmidiaceae)
Navicula (Naviculaceae)
Trachelomonas (Euglenaceae)
Diatoma (Fragilariaceae)
Netrium (Mesotaeniaceae)
Tribonema (Tribonemataceae)
Eremosphaera (Oocystaceae)
Oedogonium (Oedogoniaceae)
Ulothrix (Ulotrichaceae)
Euastrum (Desmidiaceae)
Oscillatoria (Oscillatoriaceae)
Xanthidium (Desmidiaceae)
Euglena (Euglena)
Paenium (Desmidiaceae)
Zygnema (Zygnemataceae)
Palmella (Palmellaceae) Peridinium (Peridiniaceae) Phacus (Euglenaceae)
Table 4 Growth forms of algae found in Utricularia traps in Vorarlberg and Waldviertel Vorarlberg (%)
Table 5 Taxonomy of the algae trapped by Utricularia in Vorarlberg and Waldviertel Vorarlberg (%)
Waldvierte (%)
Waldviertel (%)
Monadal
0.4
0.4
Cyanobacteria
5.5
Capsal
0.4
0.7
Bacillariophyta
0.2
5.2
Coccal
76.9
38.8
Desmidiaceae
86.3
40.9
Trichal
22.3
60.1
Zygnemataceae
3.1
32.6
Other Chlorophyta
4.5
20.0
Other algae
0.4
1.3
algae that are frequent next to the trap door without being attached can be sucked in. The bristles next to the trap door probably contribute to the enrichment of algae in this area, as suggested by Meyers and Strickler (1979). Thus, the species composition of the prey is very similar to the periphyton; Anabaena, for instance, uses to grow attached to Utricularia plants (Wagner and Mshigeni 1986) and was the most abundant Cyanophyceae among the prey as well. Mougeotia grew in high abundance on Utricularia and was trapped frequently in all study sites in Waldviertel. The percentage of algae correlates with water chemistry The percentage of algae in the prey strongly depends on the electrical conductivity of the water. In waters that are poor in ions, lots of algae were trapped,
0.0
whereas in hard or mesotrophic waters algae were rare. Utricularia minor and U. australis were found in habitats with both high and little conductivity; algae were trapped accordingly. The sites of U. vulgaris and U. bremii exhibited high conductivity; therefore, the prey contained only few algae. Unlike animal prey (Harms 1999), we found no evidence that Utricularia species with bigger traps, like U. vulgaris, would prefer larger prey algae. We therefore conclude that the differences between the investigated species are caused indirectly by different habitat preferences. This correlation may be a common feature: In Utricularia inflata WALTER from soft water with 60 lS cm-1, Gordon and Pacheco (2007) found 67% algae. According to our findings, we would have expected 64 ± 12% algae (Fig. 2). However, this
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trend was not found in U. gibba L. which grew in brackish water and still trapped huge amounts of algae. One possible reason for the preference of Utricularia from soft water sites to catch small algae is the well-known high diversity of unicellular or small filamentous algae in those fen waters (Migula 1907; Rydin and Jeglum 2006). In nutrient rich waters, filamentous algae like the branched Cladophora tend to form huge masses that are much too large to be swallowed by Utricularia bladders. Another explanation is that in many fens, increase of the electrical conductivity correlates with a gradient from poor to rich as well as with concentrations of potassium, iron and nitrogen (Rydin and Jeglum 2006; Tahvanainen 2005) Thus, hard fen waters frequently exhibit a higher productivity and nourish more herbivore animals. On the one hand, a higher abundance of animal prey is available; on the other one, they compete with Utricularia for algae. The taxonomic composition of prey in our test plants was similar to literature descriptions (Barthlott et al. 2004; Cohn 1875; Darwin 1875; Harms 2002; Juniper et al. 1989; Lloyd 1942 and many others). Here, these preferences are statistically confirmed for the first time. For neotropic Utricularia, Gordon and Placheco (2007) also stated a preference for Chlorophyta and Cyanobacteria. However, these authors found an even larger percentage of Bacillariophyta which were rare in our test plants. Unlike Hegner (1926), we found only little amounts of protozoa (3.2% of all prey) in all kinds of waters. So our results do not support the hypothesis of Mette et al. (2000) that aquatic Utricularia is specialised for the trapping of protozoa like the terrestrial species (Barthlott et al. 2004; Seine et al. 2002). Algae are trapped and killed without animals stimulating the trap According to all models published so far (Barthlott et al. 2004; Lloyd 1942; Sydenham and Findlay 1973), the mechanism of the suction trap has to be triggered by mechanical stimulation of sensitive hairs at the trap door. However, unicellular algae as found in our observations as well as by Mette et al. (2000) or Jobson et al. (2000) are much too small to bend the hairs or are even completely immobile. Therefore, the following hypotheses are taken into account:
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•
•
•
•
Algae are only sucked in by accident when the trap is stimulated by an animal (Sydenham and Findlay 1973). This hypothesis can be clearly denied according to our results: (1) More than 40% of the traps contained only algae and not a single animal. (2) If algae were only trapped together with animals, we would expect a strong correlation between the number of algae and animals in the trap, but this correlation is lacking. (3) Algae are caught not only in the natural habitat, but also under controlled conditions, without animal presence (Jobson et al. 2000). The trap is stimulated by movements of the water, maybe by touches of larger animals. During our observations, we often found large insect larvae, tadpoles, water beetles, leeches and other animals that may stimulate some traps by touching, but are too large themselves to be sucked in. Furthermore, all test plants grew next to the water surface where wind and rain may serve as mechanical stimulants. Long filamentous algae ensnarled with the trap’s bristles could facilitate this power transmission. After an elongated time without triggering, the trap sucks in water autonomously. This hypothesis is in accordance with all our observations. However, a trapping mechanism without mechanical stimulation is yet to be detected. The occurrence of algae in Utricularia traps could be an artefact due to sampling or transport. However, Gordon and Placheco (2007) found similar amounts of algae, but used another sampling protocol including immediate fixation of the traps.
In all study sites, algae were usually dead and more or less degraded. Thus, our results are in accordance with the observations of Mette et al. (2000) and Tschumpel (2002) and contradict Cohn (1875), Hegner (1926), Schumacher (1960) and Botta (1976). Probably, these early authors failed to distinguish between active traps and old, inactive or even dead ones. This may be especially true for frequent observations of Euglena living in the traps. Richards (2001) presents an image of degraded Desmidiaceae inside a bladder of Utricularia purpurea. So far, there is no direct evidence that dead algae are digested by the plant. However, Vintejoux and Ghafari (2005) as well as Płachno et al. (2006) found
Plant Ecol (2008) 199:153–162
proteases and acid phosphatases even in unfed Utricularia traps. Cyanol staining of dead algae in this study gave evidence that the plasmalemma of dead algae became completely permeable. Thus, their cytoplasm can be expected to be attacked by those omnipresent enzymes. Future aspects—the physiological role of algae In this study, we present some data on the quantitative role of algae in the prey spectrum of Utricularia. So far, it is not clear if the algae contribute to the nutrition of the plant. Plant-derived prey is well known from other carnivorous plant species: In Pinguicula lusitanica (Lentibulariaceae), flowering is enhanced by feeding with pollen grains (Harder and Zemlin 1968). Due to isotope measurements, Nepenthes ampullaria (Nepenthaceae) depends more on dead leafs collected by the pitcher traps than on animal prey (Moran et al. 2003). Rainforest species of Drosera (Droseraceae) have been suggested to utilise nutrients from canopy leaching (Lavarack 1979). Gordon and Pacheco (2007) speculate that Utricularia may gain maximum benefit from a balanced diet consisting of algae and animals. Since algae are the dominant prey organisms of Utricularia in the softest and most oligotrophic water bodies, it can be expected that algae-derived nutrients significantly contribute to the plant’s survival on these sites. On the other hand, feeding experiments so far gave no evidence for any growth support by algae. In the terrestrial U. uliginosa, both a pure diet of Euglena and Euglena intermixed with Acarina even depressed plant growth (Jobson et al. 2000.). Thus, algae even seem to be an additional stress factor wherever they form a significant percentage of prey. It should be considered that the highest percentage of algae was found next to the limit of Utricularia’s ecological range. In extreme soft water, where more than 80% algae could be expected (Fig. 2), Utricularia was not found. Furthermore, our observations offer no clear explanation for the mechanism to capture algae. Running feeding experiments excluding all mechanical movements will show if the trap is only extremely sensitive, or if we have to reconsider the trapping mechanism of Utricularia. Acknowledgements Thanks are due to Dr. I. Lang for proofreading the manuscript. Specimens of Utricularia have
161 been kindly provided by B. Schmidt and E. Mayer. K.-H. Piringer, R. Sprinzl and W. Hafellner made research in preserved areas possible. This study was supported by grant H 2130/2006 of the Hochschuljubila¨umsstiftung der Stadt Wien to M. Peroutka and grant LH-I-84/003-2005 of the Province of Niedero¨sterreich to W. Adlassnig.
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