- Email: [email protected]
Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: The role of planktonic algae
ARTICLE IN PRESS
Flora 204 (2009) 700–708 www.elsevier.de/flora
Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: The role of planktonic algae Imad Aldeen Alkhalaf, Thomas Hu¨bener, Stefan Porembski Universita¨t Rostock, Institut fu¨r Biowissenschaften, Allgemeine und Spezielle Botanik, Wismarsche Str. 8, D-18051 Rostock, Germany Received 23 July 2008; accepted 27 September 2008
Abstract The carnivorous bladderworts (Utricularia) possess complicated suction traps. Remarkably, information on the prey trapped is relatively sparse. We have conducted a detailed survey on the prey spectra found in traps of selected aquatic bladderworts (U. australis, U. vulgaris) occurring in ponds in northeastern Germany. A close examination of more than 200 traps revealed cladocerans, copepods, rotiferas, ciliates and insect larvae as being common prey. Of particular interest was the considerable amount of phytoplankton (i.e. algae, cyanobacteria) found in the traps. In total, more than 160 algae species (among others, Kirchneriella lunaris, Scenedesmus quadricauda and S. acuminatus) belonging to more than 50 genera were present, with Chlorophyceae being dominant. The role of the vegetarian diet for nutrient supply of bladderworts is discussed. r 2009 Elsevier GmbH. All rights reserved. Keywords: Algae; Bladderworts; Utricularia; Carnivorous plants; Suction bladders; Ponds
Introduction Carnivorous plants are colonizers of open habitats where macronutrients are scarce (Heslop-Harrison, 1978; Juniper et al., 1989). By definition they attract, catch and digest animals in order to meet their nutritive needs. The largest family comprising carnivorous plants is Lentibulariaceae with ca. 325 species (Mu¨ller et al., 2006) in three genera. Largest genus is Utricularia with an estimated number of 220 species with a nearly cosmopolitic distribution. The representatives of this genus in temperate zones mainly live as submerged Corresponding author.
E-mail addresses: [email protected] (I.A. Alkhalaf), [email protected] (T. Hu¨bener), [email protected] (S. Porembski). 0367-2530/$ - see front matter r 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.09.008
aquatics. Utricularia (bladderworts) exhibits extremely complex trapping devices which are known as suction bladders. For details on the morphology, anatomy and function of Utricularia traps we refer to Brugger and Rutishauser (1989), Barthlott et al. (2004) and Reifenrath et al. (2006). The prey of aquatic Utricularia species mainly consists of zooplanktic organisms (Andrikovics et al., 1988; Guisande et al., 2000; Harms, 1999; Mette et al., 2000; Sanabria-Aranda et al., 2006), and there are reports on trapped algae and cyanobacteria too (Botta, 1976; Goebel, 1891; Hegner, 1926; Lemmermann, 1914; Mette et al., 2000). But no details are available with regard to the ecological role of this latter phenomenon. It can be assumed, however, that all prey organisms (e.g. rotifers, ciliates, phytoplankton, microfungi) could provide nutrients for aquatic Utricularia species.
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
This study is aimed at giving a survey on the general prey spectrum and providing details on the trapping of algae and cyanobacteria by aquatic Utricularia species in northeast Germany. Moreover, the possible relevance of trapping planktonic algae and cyanobacteria for carnivorous bladderworts is discussed.
Material and methods The Utricularia species studied (U. australis R. Br. in the kettle holes numbered as R17, R29, U. vulgaris L. in R28, R63) occurred in four kettle holes near Rostock (Germany, Mecklenburg-Vorpommern). Trap-bearing material was collected from July to September 2005 and was transported in pond water to the laboratory. Relevant morphometric and physico-chemical parameters of the water in the kettle holes are summarized in Table 1. In total 206 traps were examined (U. australis ¼ 101 traps, U. vulgaris ¼ 105 traps). All traps were fully functional (i.e. able to trap prey) and were located on stolons and phylloclades. In the laboratory, the plants were divided into small segments with 2–3 traps per segment. Subsequently, they were conveyed to filtered pond water and fixed with acidic Lugol’s solution. The traps were washed in distilled water in order to remove epiphyton from the outer surface. Traps were opened with the help of fine needles and the content was examined under a light microscope (Zeiss Axioplan). The phytoplankton studied in the traps was over 5 mm in size. Elements of the zooplankton were subdivided into
Table 1.
701
major groups and phytoplankton was subsequently determined (identification clues: Ettl, 1978; Krammer and Lange-Bertalot, 1986–1991; Pankow, 1990; Pascher, 1925; Pestalozzi, 1982; Thienemann, 1955). Bacillariophyceae were conserved on permanent slides, embedded in Naphrax. The Utricularia traps were divided into seven size groups (following Guisande et al., 2004): 600–999, 1000–1399, 1400–1799, 1800–2199, 2200–2599, 2600–2999 and 3000–3400 mm, and the analyses of phytoplankton diversity were conducted with the help of appropriate software (SPSS, 2003, CANOCO for Windows 4.5 and ANOVA). In addition, water samples (5 ml, n ¼ 20) were taken from the kettle holes for studying the floristic composition of the phytoplankton in the vicinity of Utricularia specimens. They were preserved with acidic Lugol’s solution. Counts of the phytoplankton were carried out according to Utermo¨hl (1958) after retaining overnight and sedimentation in glass chambers.
Results Prey spectra Out of the 206 traps examined, 188 traps contained planktonic organisms. 44.7% of the traps contained both elements of zoo- and phytoplankton. 46.6% of the traps contained only phytoplankton and 8.7% of the traps were empty. The vast majority of traps of U. australis (88%) and U. vulgaris (95%) contained phytoplankton.
Mean values of physical and chemical variables of the sampled ponds, measured between July and September 2005.
Mean parameter
Latitude (N) Longitude (E) Pond length (m) Pond width (m) Pond depth (m) pH Total-P (mg L1) Orthophosphate-P (mg L1) Total-N (mmol L1) NH4-N (mmol L1) NO3-N (mmol L1) NO2-N (mmol L1) Total hardness (1dH) Carbonate hardness (1dH) Dissolved oxygen (%) Conductivity (mS/cm) Water temperature (1C)
Kettle hole number R17
R28
R29
R63
54120 600 111520 2300 68 33 1.22 5.9 244.7 92.9 271.9 14.3 0.73 0.32 1.63 0.98 34.76 79 17.7
54130 2100 111520 5100 121.5 107.5 3.22 7 80.5 9.3 142.9 7.9 0.78 0.23 2.33 1.62 110 57.11 17.5
54130 1100 111530 4400 128 96.5 0.69 7.2 28.7 1.7 306 15.7 0.86 0.25 2.34 2.81 105 89 17.6
54130 1100 111540 3400 68 51.5 1.42 6.5 46.5 9.3 81.1 3.6 0.19 0.24 5.33 4.14 63.33 107 16.1
ARTICLE IN PRESS 702
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Cladocera
R63
R29
R28
R17
100 80
(%)
60 40 20 0 Alona
Bosmina
Alonella
Disparalona
Chydorus
Pleuroxus
Fig. 1. Dominant genera of cladocera within the examined traps from four kettle holes (R17, R28, R29 and R63).
Copepoda 100
(%)
80
R63 R28
60
R29
40
R17
20 0 Cyclops
Eucyclops
Megacyclops
Themocyclops
Fig. 2. Dominant genera of copepoda within the examined traps from the four kettle holes (R17, R28, R29 and R63).
Within the examined traps different groups of zooplankton were present (i.e. ciliates, rotiferas, crustaceans and insect larvae) as well as various elements of the phytoplankton. Ciliates were dominant (60% of the zooplankton individuals) followed by crustaceans (copepods 17%, cladocerans 12% – for more details see Figs. 1 and 2), ten genera of rotifera (incl. Asplanchna, Brachionus and Lecane), insect larvae (both 4%) and other particles such as pine pollen or aquatic fungal spores (3%). Algae abundance in the traps varied largely between individual ponds and ranged between 13 and 97 individuals per trap. The phytoplankton found in the examined traps consisted of 169 species. Chlorophyceae (24 genera, in total 67 different taxa – species, subspecies, varieties) and Bacillariophyceae (18 genera, 66 taxa) were most species rich. Moreover, cyanobacteria (17 taxa), Charophyceae (12 taxa), Euglenophyceae (5 taxa) and Dinophyceae (2 taxa) occurred. Species richness of phytoplankton trapped differed between individual ponds (maximum 129 taxa, R63; minimum 46 taxa, R29). In addition, there were also differences in the dominant species, between individual ponds. In R28 Scenedesmus quadricauda and
Kirchneriella lunaris dominated, in R63 Merismopedia punctata and M. glauca, in R29 Kirchneriella lunaris and K. obesa and in R17 Dictyosphaerium chlorella and D. subsolitarium. Amongst the phytoplankton individuals trapped, Chlorophyceae (in particular the genera Scenedesmus, Kirchneriella, Dictyosphaerium, Pediastrum and Ankistrodesmus) were most abundant followed by Bacillariophyceae and cyanobacteria. Nine algae species were present in Utricularia traps of all ponds: Ankistrodesmus falcatus, Botryococcus braunii, Eudorina elegans, Monorphidium contortum, M. convolutum, Scenedesmus acuminatus, S. quadricauda, Nitzschia palea and Tabellaria flocculosa. For more details on patterns of abundance and differences between individual ponds please refer to Table 2 and Fig. 3.
Trap size The traps were more or less oval in shape and their size ranged from 670 to 3400 mm in length and from 440 to 3200 mm in height with little variation between individual ponds. On average, traps of U. vulgaris were
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Table 2. Phytoplankton species found in traps of Utricularia vulgaris (R28, R63) and U. australis (R17, R29).
Table 2. (continued ) Taxon
Taxon
703
Kettle hole
Kettle hole R17 R28 R29 R63 R17 R28 R29 R63
Bacillariophyceae Achnanthes carissima Achnanthes exigua Achnanthes minutissima Achnanthes sp. Amphora ovalis Amphora sp. Asterionella ralfsii Cyclotella distinguenda var. unipunctata Cyclotella striata Cymbella affinis Cymbella aspera Cymbella minuta Cymbella silesiaca Cymbella sp. Diatoma vulgaris Eunotia arcus Eunotia bilunaris var. mucophila Eunotia fallax Eunotia incisa Eunotia intermedia Eunotia minor Eunotia paludosa Eunotia veneris Fragilaria brevistriata Fragilaria capucina var. gracilis Fragilaria capucina var. mesolepta Fragilaria capucina Fragilaria fasciculata Fragilaria nanana Fragilaria ulna Fragilaria ulna var. acus Fragilaria ulna var. oxyrhynchus Gomphonema acuminatum Gomphonema clavatum Gomphonema constrictum Gomphonema gracile Gomphonema lingulatiforme Gomphonema olivaceum Gomphonema truncatum Navicula angusta Navicula cryptotenella Navicula heimansioides Navicula pupula Navicula radiosa Navicula schmassmannii Navicula sp. Navicula wildii Nitzschia acicularioides Nitzschia fruticosa Nitzschia gracilis Nitzschia heufleriana Nitzschia intermedia Nitzschia lorenziana
+
+
+
+ + + + + + + + +
+ + +
+
+
+ + +
+
+
+
+ +
+ +
+ + + + + + + + + + +
+
+
+ + + + + + + + + + + + + + + + + + + + + + + + + + + +
+ +
Nitzschia palea Nitzschia sigma Pinnularia divergens Pinnularia gibba Pinnularia lundii Pinnularia microstauron Stauroneis kriegerii Rhizosolenia setigera Rhopalodia gibba Stauroneis phoenicenteron Stephanodiscus neoastraea Tabellaria fenestrata Tabellaria flocculosa Charophyceae Closterium acutum var. variabile Closterium dianae Closterium moniliferum Cosmarium formosulum Cosmarium humile Cosmarium laeve Cosmarium meneghinii Cosmarium reniforme Staurastrum chaetoceras Staurastrum gracile Staurastrum paradoxum Staurastrum tetracerum Chlorophyceae Ankistrodesmus bibraianus Ankistrodesmus falcatus Ankistrodesmus fusiformis Ankistrodesmus gracilis Ankistrodesmus spiralis Botryococcus braunii Bulbochaete sp. Coelastrum microporum Coenochloris hindakii. Crucigeniella crucifera Crucigenia fenestrata Crucigenia tetrapedia Dictyosphaerium ehrenbergianum Dictyosphaerium chlorelloides Dictyosphaerium pulchellum Dictyosphaerium subsolitarium Dictyosphaerium sphagnale Didymocystis planctonica Eudorina elegans Eutetramorus fottii Golenkinia radiata Keratococcus suecius Kirchneriella aperta Kirchneriella contorta Kirchneriella dianae Kirchneriella irregularis Kirchneriella lunaris Kirchneriella obesa
+
+
+ +
+
+ + + + + +
+ + +
+ +
+ +
+
+ +
+
+ + + + + + +
+ +
+
+ + + +
+ + + +
+ +
+
+
+
+ + + +
+ +
+
+
+
+
+
+
+ + +
+
+
+
+
+ + + + + + + + + + + + + + + + + +
+ + +
+ + + +
+
+ + + +
+ +
+ + + + + +
ARTICLE IN PRESS 704
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Table 2. (continued ) Taxon
Table 2. (continued ) Kettle hole
Taxon
R17 R28 R29 R63 Kirchneriella subcapitata Monoraphidium arcuatum Monoraphidium contortum Monoraphidium convolutum Monoraphidium griffithii Monoraphidium indicum Monoraphidium komarkovae Monoraphidium minutum Nephrochlamys willeana Oedogonium sp. Oocystis parva Pandorina morum Pandorina sp. Pediastrum biradiatum var. longecornutum Pediastrum boryanum var. boryanum Pediastrum boryanum var. brevicorne Pediastrum duplex Pediastrum simplex Pediastrum tetras Quadricoccus ellipticus Quadrigula closterioides Radiococcus bavaricus Scenedesmus acuminatus Scenedesmus acutus Scenedesmus arcuatus Scenedesmus bicaudatus Scenedesmus dimorphus Scenedesmus disciformis Scenedesmus ecornis Scenedesmus granulatus f. spinosus Scenedesmus longispina Scenedesmus obtusus Scenedesmus opoliensis Scenedesmus quadricauda Scenedesmus spinosus Schroederia setigera Tetraedron incus Tetraedron minimum Tetrallantos lagerheimii Cyanobacteria Aphanocapsa delicatissima Aphanocapsa grevillei Aphanocapsa rivularis Aphanothece stagnina Chroococcus limneticus Chroococcus minutus Chroococcus turgidus Gomphosphaeria aponina Merismopedia elegans Merismopedia glauca Merismopedia punctata Microcystis aeruginosa Microcystis firma Microcystis flos-aquae
+ + + + + +
+ + +
+ +
+ +
+ + +
+
+ + + + + + + + + +
+ + +
+ + +
+
+ +
+ +
+
+ +
+ +
+
+
+
+
+
+ + +
+ +
+ +
+ + + + + + + + + + + +
+
+ + +
+ + +
+ +
Microcystis incerta Oscillatoria tenuis Synechococcus aeruginosus Dinophyceae Peridinium cinctum Peridinium umbonatum Euglenophyceae Euglena acus Euglena spirogyra Phacus longicauda Phacus pleuronectes Phacus suecicus
+
+ +
+
+
+
+ + +
+ + + +
+ + +
larger (mean length 1986 mm, max ¼ 3400 mm, min ¼ 760 mm; mean height 1536 mm, max ¼ 3400 mm, min ¼ 440 mm) than traps of U. australis (mean length 1537 mm, max ¼ 2800 mm, min ¼ 670 mm; mean height 1230 mm, max ¼ 2300 mm, min ¼ 510 mm). In general, the most frequent size class of U. vulgaris was 1400–2599 and 600–2199 mm for U. australis (Fig. 4). The number of algae trapped differed between individual size classes of traps. Most algae (93% for U. vulgaris, 85% for U. australis) were recorded in traps ranging between 1000 and 2599 mm in size. No algae were found in traps of U. vulgaris below 1000 mm in size and for U. australis above 3000 mm. For the trapped organisms the size range of phytoplankton was 15–512 mm in length and for zooplankton 331–1408 mm, while the size of the trapdoor in both Utricularia species ranged from 218 to 715 mm in length.
Water samples + +
+ + + + + + +
R17 R28 R29 R63
+
+
+
Kettle hole
+ + + + + + +
The phytoplankton analysis of the water samples resulted in a total number of 120 species (41 genera) in the four ponds with Chlorophyceae being dominant in the ponds R28, R29 and R63 whereas cyanobacteria were dominant in pond R17. With respect to number of species, the total number of species in pond R17 was 24, and 42, 49 and 84 species in the ponds R29, R28 and R63, respectively. Only three algae species were found in all four ponds: Coelatrum microporum, Scenedesmus quadricauda and Tabellaria flocculosa. A certain subset of phytoplankton species recorded in the ponds could be found in the traps. In general, over all ponds studied between 73% and 88% of the whole phytoplankton flora was found within the traps. Several algae taxa were recorded only in the traps but not in the
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Algal abundance (%)
Species abundance (%) R63 - U. vulgaris
R29 - U. australis 100
705
80 100
mean algae/cyanob p. trap 55
80
75
60
75
60
50
40
50
40
25
20
25
20
0
0
0 Chloro
Cyano
Bacill
Charo
Eugleno
Dino
R17 - U. australis mean algae/cyanob p. trap 13
100
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
R28-U. vulgaris 80 100
80
mean algae/cyanob p. trap 45
75
60
75
60
50
40
50
40
25
20
25
20
0
0
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
Species abundance (%)
Algal abundance (%)
mean algae/cyanob p. trap 97
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
Fig. 3. Relative abundance of major groups of algae/cyanobacteria, species abundance and mean total number of algae/ cyanobacteria and zooplankton per individual trap in the four kettle holes.
U.australis U.australis
U.vulgaris U.vulgaris
Frequency (%)
Frequency (%)
40
50 40
30
30
20
20
10
10
0
0
Number of algae
Number of algae
600- 1000- 1400- 1800- 2200- 2600- 3000999 1399 1799 2199 2599 2999 3400 L. (µm)
Fig. 4. Frequency (%) distribution of trap lengths of U. australis and U. vulgaris and relationships between mean number of algae per trap and trap length (mm) in the four ponds.
free water, which could be due to the sampling design (Fig. 5).
among species (ANOVA, F ¼ 32.14, po0.001) and among sites (F ¼ 44.09, po0.001), similar to the study of Harms (1999). The difference in the trap length frequency distributions among the four ponds may be because the examined traps were taken from different positions on foliage and the traps were different in age. Friday (1992) found that the trap size and their position on the plant were correlated. The ponds studied showed large differences in the average number (between 13 and 97) of phytoplankton individuals captured per trap. These numbers are higher than previously indicated by Schumacher (1960). The results showed that no relationship existed between the trap sizes of U. vulgaris and U. australis and the amount of captured phytoplankton. These results were in contrast with the previous interpretation of Friday (1991) that larger traps potentially accommodate more and larger prey. The different numbers of trapped phytoplankton among the species might be due to different phytoplankton densities in the ponds or as a consequence of differences in water chemistry.
Discussion Trap size
Trap content
The water of the ponds studied was soft and carbonate poor, and the trophic level ranged from eutrophic (R28, R63) to polytrophic (R17, R29). The analysis of trap size showed significant differences
A number of studies on the trap content of aquatic bladderworts have been conducted in the past, nearly invariably dealing with zooplankton, but almost no information was available about phytoplankton
ARTICLE IN PRESS 706
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
120
Peridiniales
Pennales
Euglenales
Centrales
Zygnematales
Volvocales
Nostocales
Oedogoniales
Chroococcales
Chlorococcales
100
(%)
80 60 40 20 0 P
T R 17
T
P R 29
T
P R 28
T
P R 63
Fig. 5. Comparison between relative abundance of the orders of phytoplankton within the traps and free water.
trapped. We found in the traps of Utricularia australis and U. vulgaris 10 genera of rotifera, 6 genera of cladocera, 4 genera of copepoda and 4 genera of ciliates. The range of size of both rotifers and ciliates was 20–420 mm, and they may feed on debris and bacteria; therefore, they possibly control the abundance and biomass of bacteria inside the traps. The microzooplankton in the traps was possibly used as a source of nutrients for carnivorous plants but this topic was out of the scope of our study. With regard to the faunistic components of the prey spectrum in traps of aquatic Utricularia species, our results largely agree with data hitherto reported (Botta, 1976; Garbini, 1899; Harms, 1999; Lim and Furtado, 1975; Mette et al., 2000; Richards, 2001; SanabriaAranda et al., 2006). It was suggested that the composition of the zooplankton trapped by aquatic Utricularia depends on habitat conditions and the availability of certain groups of organisms (Mette et al., 2000). We recorded, in addition, in the traps 169 algal taxa, belonging to six classes. The phytoplankton within the examined traps consists mainly of Chlorophyceae, Bacillariophyceae and cyanobacteria, and these observations agree with the results of Schumacher (1960) who found 25 taxa of Desmidiaceae such as Cosmarium spp., Staurastrum spp., Xanthidium spp. in the traps of Utricularia sp. Mosto (1979) found 10 species of cyanobacteria within the traps of U. oligosperma. Lemmermann (1914), Hegner (1926) and Mette et al., (2000) reported various microalgae belonging to Chlorophyceae, Euglenophyceae, Bacillariophyceae,
Charophyceae and Dinophyceae in the traps of Utricularia spp. The number of phytoplankton taxa found in the traps was higher than the number of taxa recorded in the pond water (169 vs. 120). This is certainly due to the higher study intensity devoted to the traps.
Importance of phytoplankton trapping for aquatic bladderworts Bladderworts have various glands outside and inside the traps (Chao, this journal issue), some of which secrete mucilage to allure organisms (Wallace, 1977). The captured phytoplankton individuals are microscopic free-floating organisms and cannot move by themselves. It is conceivable that they passively entered the traps during the process of zooplankton capture (Goebel, 1891) or by zooplankton excrements (Cohn, 1875). Hegner (1926) suggested that the traps do not select their prey, but any organism small enough to enter the vestibule may be captured. Certain algae (e.g. Euglena) possessing flagellae could actively move to the traps. However, there are no reports on algae being able to trigger the trap opening mechanism by themselves. It is possible that there exists a synergistic relationship between the traps of aquatic Utricularia and the captured prey. The traps might offer to phytoplankton establishment sites in an advantageous environment, and the bladderworts might benefit from the absorption of nitrogenous products released by nitrogen-fixing
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
phytoplankton, without digesting them (Wagner and Mshigeni, 1986). The mechanism of prey digestion in Utricularia is still not completely clear (Friday and Quarmby, 1994). Utricularia species possibly digest their prey by means of enzymes like phosphatases and proteases (Plachno et al., 2006; Sirova´ et al., 2003). Nitrogen-fixing planktonic cyanobacteria such as Spirulina sp. and Anabaena sp. were reported to occur on the surface and in traps of U. inflexa. But it is not known whether the bladderwort benefits from the fixed nitrogen (Wagner and Mshigeni, 1986). Moreover, perhaps the trapped phytoplankton such as Euglena sp. and Phacus sp. employ the trap as growth sites, in which they increase growing and do photosynthesis (Hegner, 1926; Mette et al., 2000). Bladderworts catch different zooplankton organisms and get more than 75% of the seasonal nitrogen demand from the captured zooplankton (Knight, 1988). U. vulgaris obtains 51.8% of its total nitrogen from captured prey (Friday and Quarmby, 1994), but it is not clear whether the capture and digestion of phytoplankton plays a necessary role for the nutrient supply of aquatic Utricularia. By using 15N-labeled phytoplankton it could be shown, at least, that Utricularia gibba takes up N from captured algae to a considerable extent (own unpublished data). Further studies are needed to quantify the exact amount of nutrients taken up by bladderworts from the trapped phytoplankton.
Acknowledgements We are thankful to S. Adler for valuable suggestions on the statistics, K. Fink, P. Kiehl and R. Paschen (all Rostock) for help during fieldwork. This study was partly supported by the Deutsche Forschungsgemeinschaft (Ba/Sp 605/9-3). Moreover, we are grateful to W. Barthlott (Bonn) for valuable hints on the topic of this study.
References Andrikovics, S., Forro´, L., Zsunics, B., 1988. The zoogenic food composition of Utricularia vulgaris in the Pond Ferto+ , Hungary. Opusc. Zool. 23, 65–70. Barthlott, W., Porembski, S., Seine, R., Theisen, I., 2004. Karnivoren: Biologie und Kultur Fleischfressender Pflanzen. Ulmer, Stuttgart. Botta, S.M., 1976. Sobre las trampas y las vı´ctimas o presas de algunas especies argentinas del ge´nero Utricularia. Darwiniana (B. Aires) 20, 127–154. Brugger, J., Rutishauser, R., 1989. Bau und Entwicklung landbewohnender Utricularia-Arten. Bot. Helv. 99, 91–146. Cohn, F., 1875. Ueber die Function der Blasen von Aldrovanda und Utricularia. Cohn’s Beitr. Biol. Pflanz. 1, 71–92.
707
Ettl, H., 1978. Xanthophyceae. In: Ettl, L., Gerloff, J., Heynig, H. (Eds.), Su¨ßwasserflora von Mitteleuropa, vol. 3 (1). Gustav Fischer, Stuttgart. Friday, L.E., 1991. The size and shape of traps of Utricularia vulgaris L. Funct. Ecol. 5, 602–607. Friday, L.E., 1992. Measuring investment in carnivory: seasonal and individual variation in trap number and biomass in Utricularia vulgaris L. New Phytol. 121, 439–445. Friday, L., Quarmby, C., 1994. Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L. New Phytol. 126, 273–281. Garbini, A., 1899. Le vittime della Utricularia neglecta. Atti Reale 1st. Veneto 58. Goebel, K., 1891. Morphologische und biologische Studien. V. Ann. Jard. bot. Buitenzorg 9, 41–119. Guisande, C., Aranguren, N., Arande-Sossa, C., Prat, N., Granado-Lorencio, C., Barrios, M.L., Bolivar, A., Avellaneda, M.N., Duque, R.S., 2004. Relative balance of the cost and benefit associated with carnivory in the tropical Utricularia foliosa. Aquat. Bot. 80, 271–282. Guisande, C., Andrade, C., Granado-Lorencio, C., Duque, S.R., Avellaneda, M., 2000. Effect of zooplankton and conductivity on tropical Utricularia foliosa investment in carnivory. Aquat. Ecol. 34, 137–142. Harms, S., 1999. Prey selection in three species of the carnivorous aquatic plant Utricularia (bladderwort). Arch. Hydrobiol. 146, 449–470. Hegner, R.W., 1926. The interrelations of protozoa and the utricles of Utricularia. Biol. Bull. 50, 239–270. Heslop-Harrison, Y., 1978. Carnivorous plants. Sci. Am. 238, 102–111. Juniper, B.E., Robins, R.J., Joel, M.D., 1989. The Carnivorous Plants. Academic Press, London. Krammer, H., Lange-Bertalot, H., 1986–1991. Bacillariophyceae. In: Ettl, H., Gerloff, J., Heynig, Mollenhauer., D. (Eds.), Su¨ßwasserflora von Mitteleuropa, vol. 2 (1–4). Gustav Fischer, Stuttgart. Knight, S.E., 1988. The ecophysiological significance of carnivory in Utricularia vulgaris. Dissertation. University of Wisconsin, Madison, Wisconsin, USA. Lemmermann, E., 1914. Algologische Beitra¨ge 23. U¨ber das Vorkommen von Algen in den Schla¨uchen von Utricularia. Abh. Nat. Ver. Bremen 23, 261–267. Lim, R.P., Furtado, J.I., 1975. Population changes in the aquatic fauna inhabiting the bladderwort, Utricularia flexuosa Vahl, in a tropical swamp, Tasek Bera, Malaysia. Verh. Int. Ver. Limnol. 19, 1390–1397. Mette, N., Wilbert, N., Barthlott, W., 2000. Food composition of aquatic bladderworts (Utricularia, Lentibulariaceae) in various habitats. Beitr. Biol. Pflanz. 172, 65–73. Mosto, P., 1979. Algas en trampas de Utricularia oligosperma. Bol. Soc. Argent. Bot. 18, 89–100. Mu¨ller, K.F., Borsch, T., Legendre, L., Porembski, S., Barthlott, W., 2006. Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. 8, 748–757. Pankow, H., 1990. Ostsee – Algenflora. G. Fischer, Jena. Pascher, A., 1925. Die Su¨ßwasser – Flora Deutschlands, ¨ sterreichs und der Schweiz. G. Fischer, Jena. O
ARTICLE IN PRESS 708
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Pestalozzi, H., 1982. Das Phytoplankton des Su¨ßwassers. E. Schweizerbart, Stuttgart. Plachno, B.J., Adamec, L., Lichtscheidl, I.K., Peroutka, M., Adlassing, W., Vrba, J., 2006. Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. 8, 813–820. Reifenrath, K., Theisen, I., Schnitzler, J., Porembski, S., Barthlott, W., 2006. Trap architecture in carnivorous Utricularia (Lentibulariaceae). Flora 201, 597–605. Richards, J.H., 2001. Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? Am. J. Bot. 88, 170–176. Sanabria-Aranda, L., Gonza´lez-Bermu´dez, A., Torres, N.N., Guisande, C., Manjare´s-Herna´ndez, A., Valoyes-Valois, V., Dı´az-Olarte, J., Andrade-Sossa, C., Duque, S.R., 2006. Predation by the tropical plant Utricularia foliosa. Freshwater Biol. 51, 1999–2008.
Schumacher, G.J., 1960. Further notes on the occurrence of Desmids in Utricularia bladders. Castanea 25, 62–65. Sirova´, D., Adamec, L., Vrba, J., 2003. Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytol. 159, 669–675. Thienemann, A., 1955. Die Binnengewa¨sser. E. Schweizerbart, Stuttgart. Utermo¨hl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplanktonmethodik. Mitt. Int. Verh. Limnol. 9, 1–38. Wagner, G.M., Mshigeni, K.E., 1986. The Utricularia–Cyanophyta association and its nitrogen-fixing capacity. Hydrobiologia 141, 255–261. Wallace, L.R., 1977. Substrate discrimination by larvae of the sessile rotifer Ptygura beauchampi Edmondson. Freshwater Biol. 7, 301–309.
Flora 204 (2009) 700–708 www.elsevier.de/flora
Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: The role of planktonic algae Imad Aldeen Alkhalaf, Thomas Hu¨bener, Stefan Porembski Universita¨t Rostock, Institut fu¨r Biowissenschaften, Allgemeine und Spezielle Botanik, Wismarsche Str. 8, D-18051 Rostock, Germany Received 23 July 2008; accepted 27 September 2008
Abstract The carnivorous bladderworts (Utricularia) possess complicated suction traps. Remarkably, information on the prey trapped is relatively sparse. We have conducted a detailed survey on the prey spectra found in traps of selected aquatic bladderworts (U. australis, U. vulgaris) occurring in ponds in northeastern Germany. A close examination of more than 200 traps revealed cladocerans, copepods, rotiferas, ciliates and insect larvae as being common prey. Of particular interest was the considerable amount of phytoplankton (i.e. algae, cyanobacteria) found in the traps. In total, more than 160 algae species (among others, Kirchneriella lunaris, Scenedesmus quadricauda and S. acuminatus) belonging to more than 50 genera were present, with Chlorophyceae being dominant. The role of the vegetarian diet for nutrient supply of bladderworts is discussed. r 2009 Elsevier GmbH. All rights reserved. Keywords: Algae; Bladderworts; Utricularia; Carnivorous plants; Suction bladders; Ponds
Introduction Carnivorous plants are colonizers of open habitats where macronutrients are scarce (Heslop-Harrison, 1978; Juniper et al., 1989). By definition they attract, catch and digest animals in order to meet their nutritive needs. The largest family comprising carnivorous plants is Lentibulariaceae with ca. 325 species (Mu¨ller et al., 2006) in three genera. Largest genus is Utricularia with an estimated number of 220 species with a nearly cosmopolitic distribution. The representatives of this genus in temperate zones mainly live as submerged Corresponding author.
E-mail addresses: [email protected] (I.A. Alkhalaf), [email protected] (T. Hu¨bener), [email protected] (S. Porembski). 0367-2530/$ - see front matter r 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.09.008
aquatics. Utricularia (bladderworts) exhibits extremely complex trapping devices which are known as suction bladders. For details on the morphology, anatomy and function of Utricularia traps we refer to Brugger and Rutishauser (1989), Barthlott et al. (2004) and Reifenrath et al. (2006). The prey of aquatic Utricularia species mainly consists of zooplanktic organisms (Andrikovics et al., 1988; Guisande et al., 2000; Harms, 1999; Mette et al., 2000; Sanabria-Aranda et al., 2006), and there are reports on trapped algae and cyanobacteria too (Botta, 1976; Goebel, 1891; Hegner, 1926; Lemmermann, 1914; Mette et al., 2000). But no details are available with regard to the ecological role of this latter phenomenon. It can be assumed, however, that all prey organisms (e.g. rotifers, ciliates, phytoplankton, microfungi) could provide nutrients for aquatic Utricularia species.
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
This study is aimed at giving a survey on the general prey spectrum and providing details on the trapping of algae and cyanobacteria by aquatic Utricularia species in northeast Germany. Moreover, the possible relevance of trapping planktonic algae and cyanobacteria for carnivorous bladderworts is discussed.
Material and methods The Utricularia species studied (U. australis R. Br. in the kettle holes numbered as R17, R29, U. vulgaris L. in R28, R63) occurred in four kettle holes near Rostock (Germany, Mecklenburg-Vorpommern). Trap-bearing material was collected from July to September 2005 and was transported in pond water to the laboratory. Relevant morphometric and physico-chemical parameters of the water in the kettle holes are summarized in Table 1. In total 206 traps were examined (U. australis ¼ 101 traps, U. vulgaris ¼ 105 traps). All traps were fully functional (i.e. able to trap prey) and were located on stolons and phylloclades. In the laboratory, the plants were divided into small segments with 2–3 traps per segment. Subsequently, they were conveyed to filtered pond water and fixed with acidic Lugol’s solution. The traps were washed in distilled water in order to remove epiphyton from the outer surface. Traps were opened with the help of fine needles and the content was examined under a light microscope (Zeiss Axioplan). The phytoplankton studied in the traps was over 5 mm in size. Elements of the zooplankton were subdivided into
Table 1.
701
major groups and phytoplankton was subsequently determined (identification clues: Ettl, 1978; Krammer and Lange-Bertalot, 1986–1991; Pankow, 1990; Pascher, 1925; Pestalozzi, 1982; Thienemann, 1955). Bacillariophyceae were conserved on permanent slides, embedded in Naphrax. The Utricularia traps were divided into seven size groups (following Guisande et al., 2004): 600–999, 1000–1399, 1400–1799, 1800–2199, 2200–2599, 2600–2999 and 3000–3400 mm, and the analyses of phytoplankton diversity were conducted with the help of appropriate software (SPSS, 2003, CANOCO for Windows 4.5 and ANOVA). In addition, water samples (5 ml, n ¼ 20) were taken from the kettle holes for studying the floristic composition of the phytoplankton in the vicinity of Utricularia specimens. They were preserved with acidic Lugol’s solution. Counts of the phytoplankton were carried out according to Utermo¨hl (1958) after retaining overnight and sedimentation in glass chambers.
Results Prey spectra Out of the 206 traps examined, 188 traps contained planktonic organisms. 44.7% of the traps contained both elements of zoo- and phytoplankton. 46.6% of the traps contained only phytoplankton and 8.7% of the traps were empty. The vast majority of traps of U. australis (88%) and U. vulgaris (95%) contained phytoplankton.
Mean values of physical and chemical variables of the sampled ponds, measured between July and September 2005.
Mean parameter
Latitude (N) Longitude (E) Pond length (m) Pond width (m) Pond depth (m) pH Total-P (mg L1) Orthophosphate-P (mg L1) Total-N (mmol L1) NH4-N (mmol L1) NO3-N (mmol L1) NO2-N (mmol L1) Total hardness (1dH) Carbonate hardness (1dH) Dissolved oxygen (%) Conductivity (mS/cm) Water temperature (1C)
Kettle hole number R17
R28
R29
R63
54120 600 111520 2300 68 33 1.22 5.9 244.7 92.9 271.9 14.3 0.73 0.32 1.63 0.98 34.76 79 17.7
54130 2100 111520 5100 121.5 107.5 3.22 7 80.5 9.3 142.9 7.9 0.78 0.23 2.33 1.62 110 57.11 17.5
54130 1100 111530 4400 128 96.5 0.69 7.2 28.7 1.7 306 15.7 0.86 0.25 2.34 2.81 105 89 17.6
54130 1100 111540 3400 68 51.5 1.42 6.5 46.5 9.3 81.1 3.6 0.19 0.24 5.33 4.14 63.33 107 16.1
ARTICLE IN PRESS 702
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Cladocera
R63
R29
R28
R17
100 80
(%)
60 40 20 0 Alona
Bosmina
Alonella
Disparalona
Chydorus
Pleuroxus
Fig. 1. Dominant genera of cladocera within the examined traps from four kettle holes (R17, R28, R29 and R63).
Copepoda 100
(%)
80
R63 R28
60
R29
40
R17
20 0 Cyclops
Eucyclops
Megacyclops
Themocyclops
Fig. 2. Dominant genera of copepoda within the examined traps from the four kettle holes (R17, R28, R29 and R63).
Within the examined traps different groups of zooplankton were present (i.e. ciliates, rotiferas, crustaceans and insect larvae) as well as various elements of the phytoplankton. Ciliates were dominant (60% of the zooplankton individuals) followed by crustaceans (copepods 17%, cladocerans 12% – for more details see Figs. 1 and 2), ten genera of rotifera (incl. Asplanchna, Brachionus and Lecane), insect larvae (both 4%) and other particles such as pine pollen or aquatic fungal spores (3%). Algae abundance in the traps varied largely between individual ponds and ranged between 13 and 97 individuals per trap. The phytoplankton found in the examined traps consisted of 169 species. Chlorophyceae (24 genera, in total 67 different taxa – species, subspecies, varieties) and Bacillariophyceae (18 genera, 66 taxa) were most species rich. Moreover, cyanobacteria (17 taxa), Charophyceae (12 taxa), Euglenophyceae (5 taxa) and Dinophyceae (2 taxa) occurred. Species richness of phytoplankton trapped differed between individual ponds (maximum 129 taxa, R63; minimum 46 taxa, R29). In addition, there were also differences in the dominant species, between individual ponds. In R28 Scenedesmus quadricauda and
Kirchneriella lunaris dominated, in R63 Merismopedia punctata and M. glauca, in R29 Kirchneriella lunaris and K. obesa and in R17 Dictyosphaerium chlorella and D. subsolitarium. Amongst the phytoplankton individuals trapped, Chlorophyceae (in particular the genera Scenedesmus, Kirchneriella, Dictyosphaerium, Pediastrum and Ankistrodesmus) were most abundant followed by Bacillariophyceae and cyanobacteria. Nine algae species were present in Utricularia traps of all ponds: Ankistrodesmus falcatus, Botryococcus braunii, Eudorina elegans, Monorphidium contortum, M. convolutum, Scenedesmus acuminatus, S. quadricauda, Nitzschia palea and Tabellaria flocculosa. For more details on patterns of abundance and differences between individual ponds please refer to Table 2 and Fig. 3.
Trap size The traps were more or less oval in shape and their size ranged from 670 to 3400 mm in length and from 440 to 3200 mm in height with little variation between individual ponds. On average, traps of U. vulgaris were
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Table 2. Phytoplankton species found in traps of Utricularia vulgaris (R28, R63) and U. australis (R17, R29).
Table 2. (continued ) Taxon
Taxon
703
Kettle hole
Kettle hole R17 R28 R29 R63 R17 R28 R29 R63
Bacillariophyceae Achnanthes carissima Achnanthes exigua Achnanthes minutissima Achnanthes sp. Amphora ovalis Amphora sp. Asterionella ralfsii Cyclotella distinguenda var. unipunctata Cyclotella striata Cymbella affinis Cymbella aspera Cymbella minuta Cymbella silesiaca Cymbella sp. Diatoma vulgaris Eunotia arcus Eunotia bilunaris var. mucophila Eunotia fallax Eunotia incisa Eunotia intermedia Eunotia minor Eunotia paludosa Eunotia veneris Fragilaria brevistriata Fragilaria capucina var. gracilis Fragilaria capucina var. mesolepta Fragilaria capucina Fragilaria fasciculata Fragilaria nanana Fragilaria ulna Fragilaria ulna var. acus Fragilaria ulna var. oxyrhynchus Gomphonema acuminatum Gomphonema clavatum Gomphonema constrictum Gomphonema gracile Gomphonema lingulatiforme Gomphonema olivaceum Gomphonema truncatum Navicula angusta Navicula cryptotenella Navicula heimansioides Navicula pupula Navicula radiosa Navicula schmassmannii Navicula sp. Navicula wildii Nitzschia acicularioides Nitzschia fruticosa Nitzschia gracilis Nitzschia heufleriana Nitzschia intermedia Nitzschia lorenziana
+
+
+
+ + + + + + + + +
+ + +
+
+
+ + +
+
+
+
+ +
+ +
+ + + + + + + + + + +
+
+
+ + + + + + + + + + + + + + + + + + + + + + + + + + + +
+ +
Nitzschia palea Nitzschia sigma Pinnularia divergens Pinnularia gibba Pinnularia lundii Pinnularia microstauron Stauroneis kriegerii Rhizosolenia setigera Rhopalodia gibba Stauroneis phoenicenteron Stephanodiscus neoastraea Tabellaria fenestrata Tabellaria flocculosa Charophyceae Closterium acutum var. variabile Closterium dianae Closterium moniliferum Cosmarium formosulum Cosmarium humile Cosmarium laeve Cosmarium meneghinii Cosmarium reniforme Staurastrum chaetoceras Staurastrum gracile Staurastrum paradoxum Staurastrum tetracerum Chlorophyceae Ankistrodesmus bibraianus Ankistrodesmus falcatus Ankistrodesmus fusiformis Ankistrodesmus gracilis Ankistrodesmus spiralis Botryococcus braunii Bulbochaete sp. Coelastrum microporum Coenochloris hindakii. Crucigeniella crucifera Crucigenia fenestrata Crucigenia tetrapedia Dictyosphaerium ehrenbergianum Dictyosphaerium chlorelloides Dictyosphaerium pulchellum Dictyosphaerium subsolitarium Dictyosphaerium sphagnale Didymocystis planctonica Eudorina elegans Eutetramorus fottii Golenkinia radiata Keratococcus suecius Kirchneriella aperta Kirchneriella contorta Kirchneriella dianae Kirchneriella irregularis Kirchneriella lunaris Kirchneriella obesa
+
+
+ +
+
+ + + + + +
+ + +
+ +
+ +
+
+ +
+
+ + + + + + +
+ +
+
+ + + +
+ + + +
+ +
+
+
+
+ + + +
+ +
+
+
+
+
+
+
+ + +
+
+
+
+
+ + + + + + + + + + + + + + + + + +
+ + +
+ + + +
+
+ + + +
+ +
+ + + + + +
ARTICLE IN PRESS 704
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Table 2. (continued ) Taxon
Table 2. (continued ) Kettle hole
Taxon
R17 R28 R29 R63 Kirchneriella subcapitata Monoraphidium arcuatum Monoraphidium contortum Monoraphidium convolutum Monoraphidium griffithii Monoraphidium indicum Monoraphidium komarkovae Monoraphidium minutum Nephrochlamys willeana Oedogonium sp. Oocystis parva Pandorina morum Pandorina sp. Pediastrum biradiatum var. longecornutum Pediastrum boryanum var. boryanum Pediastrum boryanum var. brevicorne Pediastrum duplex Pediastrum simplex Pediastrum tetras Quadricoccus ellipticus Quadrigula closterioides Radiococcus bavaricus Scenedesmus acuminatus Scenedesmus acutus Scenedesmus arcuatus Scenedesmus bicaudatus Scenedesmus dimorphus Scenedesmus disciformis Scenedesmus ecornis Scenedesmus granulatus f. spinosus Scenedesmus longispina Scenedesmus obtusus Scenedesmus opoliensis Scenedesmus quadricauda Scenedesmus spinosus Schroederia setigera Tetraedron incus Tetraedron minimum Tetrallantos lagerheimii Cyanobacteria Aphanocapsa delicatissima Aphanocapsa grevillei Aphanocapsa rivularis Aphanothece stagnina Chroococcus limneticus Chroococcus minutus Chroococcus turgidus Gomphosphaeria aponina Merismopedia elegans Merismopedia glauca Merismopedia punctata Microcystis aeruginosa Microcystis firma Microcystis flos-aquae
+ + + + + +
+ + +
+ +
+ +
+ + +
+
+ + + + + + + + + +
+ + +
+ + +
+
+ +
+ +
+
+ +
+ +
+
+
+
+
+
+ + +
+ +
+ +
+ + + + + + + + + + + +
+
+ + +
+ + +
+ +
Microcystis incerta Oscillatoria tenuis Synechococcus aeruginosus Dinophyceae Peridinium cinctum Peridinium umbonatum Euglenophyceae Euglena acus Euglena spirogyra Phacus longicauda Phacus pleuronectes Phacus suecicus
+
+ +
+
+
+
+ + +
+ + + +
+ + +
larger (mean length 1986 mm, max ¼ 3400 mm, min ¼ 760 mm; mean height 1536 mm, max ¼ 3400 mm, min ¼ 440 mm) than traps of U. australis (mean length 1537 mm, max ¼ 2800 mm, min ¼ 670 mm; mean height 1230 mm, max ¼ 2300 mm, min ¼ 510 mm). In general, the most frequent size class of U. vulgaris was 1400–2599 and 600–2199 mm for U. australis (Fig. 4). The number of algae trapped differed between individual size classes of traps. Most algae (93% for U. vulgaris, 85% for U. australis) were recorded in traps ranging between 1000 and 2599 mm in size. No algae were found in traps of U. vulgaris below 1000 mm in size and for U. australis above 3000 mm. For the trapped organisms the size range of phytoplankton was 15–512 mm in length and for zooplankton 331–1408 mm, while the size of the trapdoor in both Utricularia species ranged from 218 to 715 mm in length.
Water samples + +
+ + + + + + +
R17 R28 R29 R63
+
+
+
Kettle hole
+ + + + + + +
The phytoplankton analysis of the water samples resulted in a total number of 120 species (41 genera) in the four ponds with Chlorophyceae being dominant in the ponds R28, R29 and R63 whereas cyanobacteria were dominant in pond R17. With respect to number of species, the total number of species in pond R17 was 24, and 42, 49 and 84 species in the ponds R29, R28 and R63, respectively. Only three algae species were found in all four ponds: Coelatrum microporum, Scenedesmus quadricauda and Tabellaria flocculosa. A certain subset of phytoplankton species recorded in the ponds could be found in the traps. In general, over all ponds studied between 73% and 88% of the whole phytoplankton flora was found within the traps. Several algae taxa were recorded only in the traps but not in the
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Algal abundance (%)
Species abundance (%) R63 - U. vulgaris
R29 - U. australis 100
705
80 100
mean algae/cyanob p. trap 55
80
75
60
75
60
50
40
50
40
25
20
25
20
0
0
0 Chloro
Cyano
Bacill
Charo
Eugleno
Dino
R17 - U. australis mean algae/cyanob p. trap 13
100
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
R28-U. vulgaris 80 100
80
mean algae/cyanob p. trap 45
75
60
75
60
50
40
50
40
25
20
25
20
0
0
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
Species abundance (%)
Algal abundance (%)
mean algae/cyanob p. trap 97
0 Chloro
Bacill
Cyano
Charo
Eugleno
Dino
Fig. 3. Relative abundance of major groups of algae/cyanobacteria, species abundance and mean total number of algae/ cyanobacteria and zooplankton per individual trap in the four kettle holes.
U.australis U.australis
U.vulgaris U.vulgaris
Frequency (%)
Frequency (%)
40
50 40
30
30
20
20
10
10
0
0
Number of algae
Number of algae
600- 1000- 1400- 1800- 2200- 2600- 3000999 1399 1799 2199 2599 2999 3400 L. (µm)
Fig. 4. Frequency (%) distribution of trap lengths of U. australis and U. vulgaris and relationships between mean number of algae per trap and trap length (mm) in the four ponds.
free water, which could be due to the sampling design (Fig. 5).
among species (ANOVA, F ¼ 32.14, po0.001) and among sites (F ¼ 44.09, po0.001), similar to the study of Harms (1999). The difference in the trap length frequency distributions among the four ponds may be because the examined traps were taken from different positions on foliage and the traps were different in age. Friday (1992) found that the trap size and their position on the plant were correlated. The ponds studied showed large differences in the average number (between 13 and 97) of phytoplankton individuals captured per trap. These numbers are higher than previously indicated by Schumacher (1960). The results showed that no relationship existed between the trap sizes of U. vulgaris and U. australis and the amount of captured phytoplankton. These results were in contrast with the previous interpretation of Friday (1991) that larger traps potentially accommodate more and larger prey. The different numbers of trapped phytoplankton among the species might be due to different phytoplankton densities in the ponds or as a consequence of differences in water chemistry.
Discussion Trap size
Trap content
The water of the ponds studied was soft and carbonate poor, and the trophic level ranged from eutrophic (R28, R63) to polytrophic (R17, R29). The analysis of trap size showed significant differences
A number of studies on the trap content of aquatic bladderworts have been conducted in the past, nearly invariably dealing with zooplankton, but almost no information was available about phytoplankton
ARTICLE IN PRESS 706
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
120
Peridiniales
Pennales
Euglenales
Centrales
Zygnematales
Volvocales
Nostocales
Oedogoniales
Chroococcales
Chlorococcales
100
(%)
80 60 40 20 0 P
T R 17
T
P R 29
T
P R 28
T
P R 63
Fig. 5. Comparison between relative abundance of the orders of phytoplankton within the traps and free water.
trapped. We found in the traps of Utricularia australis and U. vulgaris 10 genera of rotifera, 6 genera of cladocera, 4 genera of copepoda and 4 genera of ciliates. The range of size of both rotifers and ciliates was 20–420 mm, and they may feed on debris and bacteria; therefore, they possibly control the abundance and biomass of bacteria inside the traps. The microzooplankton in the traps was possibly used as a source of nutrients for carnivorous plants but this topic was out of the scope of our study. With regard to the faunistic components of the prey spectrum in traps of aquatic Utricularia species, our results largely agree with data hitherto reported (Botta, 1976; Garbini, 1899; Harms, 1999; Lim and Furtado, 1975; Mette et al., 2000; Richards, 2001; SanabriaAranda et al., 2006). It was suggested that the composition of the zooplankton trapped by aquatic Utricularia depends on habitat conditions and the availability of certain groups of organisms (Mette et al., 2000). We recorded, in addition, in the traps 169 algal taxa, belonging to six classes. The phytoplankton within the examined traps consists mainly of Chlorophyceae, Bacillariophyceae and cyanobacteria, and these observations agree with the results of Schumacher (1960) who found 25 taxa of Desmidiaceae such as Cosmarium spp., Staurastrum spp., Xanthidium spp. in the traps of Utricularia sp. Mosto (1979) found 10 species of cyanobacteria within the traps of U. oligosperma. Lemmermann (1914), Hegner (1926) and Mette et al., (2000) reported various microalgae belonging to Chlorophyceae, Euglenophyceae, Bacillariophyceae,
Charophyceae and Dinophyceae in the traps of Utricularia spp. The number of phytoplankton taxa found in the traps was higher than the number of taxa recorded in the pond water (169 vs. 120). This is certainly due to the higher study intensity devoted to the traps.
Importance of phytoplankton trapping for aquatic bladderworts Bladderworts have various glands outside and inside the traps (Chao, this journal issue), some of which secrete mucilage to allure organisms (Wallace, 1977). The captured phytoplankton individuals are microscopic free-floating organisms and cannot move by themselves. It is conceivable that they passively entered the traps during the process of zooplankton capture (Goebel, 1891) or by zooplankton excrements (Cohn, 1875). Hegner (1926) suggested that the traps do not select their prey, but any organism small enough to enter the vestibule may be captured. Certain algae (e.g. Euglena) possessing flagellae could actively move to the traps. However, there are no reports on algae being able to trigger the trap opening mechanism by themselves. It is possible that there exists a synergistic relationship between the traps of aquatic Utricularia and the captured prey. The traps might offer to phytoplankton establishment sites in an advantageous environment, and the bladderworts might benefit from the absorption of nitrogenous products released by nitrogen-fixing
ARTICLE IN PRESS I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
phytoplankton, without digesting them (Wagner and Mshigeni, 1986). The mechanism of prey digestion in Utricularia is still not completely clear (Friday and Quarmby, 1994). Utricularia species possibly digest their prey by means of enzymes like phosphatases and proteases (Plachno et al., 2006; Sirova´ et al., 2003). Nitrogen-fixing planktonic cyanobacteria such as Spirulina sp. and Anabaena sp. were reported to occur on the surface and in traps of U. inflexa. But it is not known whether the bladderwort benefits from the fixed nitrogen (Wagner and Mshigeni, 1986). Moreover, perhaps the trapped phytoplankton such as Euglena sp. and Phacus sp. employ the trap as growth sites, in which they increase growing and do photosynthesis (Hegner, 1926; Mette et al., 2000). Bladderworts catch different zooplankton organisms and get more than 75% of the seasonal nitrogen demand from the captured zooplankton (Knight, 1988). U. vulgaris obtains 51.8% of its total nitrogen from captured prey (Friday and Quarmby, 1994), but it is not clear whether the capture and digestion of phytoplankton plays a necessary role for the nutrient supply of aquatic Utricularia. By using 15N-labeled phytoplankton it could be shown, at least, that Utricularia gibba takes up N from captured algae to a considerable extent (own unpublished data). Further studies are needed to quantify the exact amount of nutrients taken up by bladderworts from the trapped phytoplankton.
Acknowledgements We are thankful to S. Adler for valuable suggestions on the statistics, K. Fink, P. Kiehl and R. Paschen (all Rostock) for help during fieldwork. This study was partly supported by the Deutsche Forschungsgemeinschaft (Ba/Sp 605/9-3). Moreover, we are grateful to W. Barthlott (Bonn) for valuable hints on the topic of this study.
References Andrikovics, S., Forro´, L., Zsunics, B., 1988. The zoogenic food composition of Utricularia vulgaris in the Pond Ferto+ , Hungary. Opusc. Zool. 23, 65–70. Barthlott, W., Porembski, S., Seine, R., Theisen, I., 2004. Karnivoren: Biologie und Kultur Fleischfressender Pflanzen. Ulmer, Stuttgart. Botta, S.M., 1976. Sobre las trampas y las vı´ctimas o presas de algunas especies argentinas del ge´nero Utricularia. Darwiniana (B. Aires) 20, 127–154. Brugger, J., Rutishauser, R., 1989. Bau und Entwicklung landbewohnender Utricularia-Arten. Bot. Helv. 99, 91–146. Cohn, F., 1875. Ueber die Function der Blasen von Aldrovanda und Utricularia. Cohn’s Beitr. Biol. Pflanz. 1, 71–92.
707
Ettl, H., 1978. Xanthophyceae. In: Ettl, L., Gerloff, J., Heynig, H. (Eds.), Su¨ßwasserflora von Mitteleuropa, vol. 3 (1). Gustav Fischer, Stuttgart. Friday, L.E., 1991. The size and shape of traps of Utricularia vulgaris L. Funct. Ecol. 5, 602–607. Friday, L.E., 1992. Measuring investment in carnivory: seasonal and individual variation in trap number and biomass in Utricularia vulgaris L. New Phytol. 121, 439–445. Friday, L., Quarmby, C., 1994. Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L. New Phytol. 126, 273–281. Garbini, A., 1899. Le vittime della Utricularia neglecta. Atti Reale 1st. Veneto 58. Goebel, K., 1891. Morphologische und biologische Studien. V. Ann. Jard. bot. Buitenzorg 9, 41–119. Guisande, C., Aranguren, N., Arande-Sossa, C., Prat, N., Granado-Lorencio, C., Barrios, M.L., Bolivar, A., Avellaneda, M.N., Duque, R.S., 2004. Relative balance of the cost and benefit associated with carnivory in the tropical Utricularia foliosa. Aquat. Bot. 80, 271–282. Guisande, C., Andrade, C., Granado-Lorencio, C., Duque, S.R., Avellaneda, M., 2000. Effect of zooplankton and conductivity on tropical Utricularia foliosa investment in carnivory. Aquat. Ecol. 34, 137–142. Harms, S., 1999. Prey selection in three species of the carnivorous aquatic plant Utricularia (bladderwort). Arch. Hydrobiol. 146, 449–470. Hegner, R.W., 1926. The interrelations of protozoa and the utricles of Utricularia. Biol. Bull. 50, 239–270. Heslop-Harrison, Y., 1978. Carnivorous plants. Sci. Am. 238, 102–111. Juniper, B.E., Robins, R.J., Joel, M.D., 1989. The Carnivorous Plants. Academic Press, London. Krammer, H., Lange-Bertalot, H., 1986–1991. Bacillariophyceae. In: Ettl, H., Gerloff, J., Heynig, Mollenhauer., D. (Eds.), Su¨ßwasserflora von Mitteleuropa, vol. 2 (1–4). Gustav Fischer, Stuttgart. Knight, S.E., 1988. The ecophysiological significance of carnivory in Utricularia vulgaris. Dissertation. University of Wisconsin, Madison, Wisconsin, USA. Lemmermann, E., 1914. Algologische Beitra¨ge 23. U¨ber das Vorkommen von Algen in den Schla¨uchen von Utricularia. Abh. Nat. Ver. Bremen 23, 261–267. Lim, R.P., Furtado, J.I., 1975. Population changes in the aquatic fauna inhabiting the bladderwort, Utricularia flexuosa Vahl, in a tropical swamp, Tasek Bera, Malaysia. Verh. Int. Ver. Limnol. 19, 1390–1397. Mette, N., Wilbert, N., Barthlott, W., 2000. Food composition of aquatic bladderworts (Utricularia, Lentibulariaceae) in various habitats. Beitr. Biol. Pflanz. 172, 65–73. Mosto, P., 1979. Algas en trampas de Utricularia oligosperma. Bol. Soc. Argent. Bot. 18, 89–100. Mu¨ller, K.F., Borsch, T., Legendre, L., Porembski, S., Barthlott, W., 2006. Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. 8, 748–757. Pankow, H., 1990. Ostsee – Algenflora. G. Fischer, Jena. Pascher, A., 1925. Die Su¨ßwasser – Flora Deutschlands, ¨ sterreichs und der Schweiz. G. Fischer, Jena. O
ARTICLE IN PRESS 708
I.A. Alkhalaf et al. / Flora 204 (2009) 700–708
Pestalozzi, H., 1982. Das Phytoplankton des Su¨ßwassers. E. Schweizerbart, Stuttgart. Plachno, B.J., Adamec, L., Lichtscheidl, I.K., Peroutka, M., Adlassing, W., Vrba, J., 2006. Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. 8, 813–820. Reifenrath, K., Theisen, I., Schnitzler, J., Porembski, S., Barthlott, W., 2006. Trap architecture in carnivorous Utricularia (Lentibulariaceae). Flora 201, 597–605. Richards, J.H., 2001. Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? Am. J. Bot. 88, 170–176. Sanabria-Aranda, L., Gonza´lez-Bermu´dez, A., Torres, N.N., Guisande, C., Manjare´s-Herna´ndez, A., Valoyes-Valois, V., Dı´az-Olarte, J., Andrade-Sossa, C., Duque, S.R., 2006. Predation by the tropical plant Utricularia foliosa. Freshwater Biol. 51, 1999–2008.
Schumacher, G.J., 1960. Further notes on the occurrence of Desmids in Utricularia bladders. Castanea 25, 62–65. Sirova´, D., Adamec, L., Vrba, J., 2003. Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytol. 159, 669–675. Thienemann, A., 1955. Die Binnengewa¨sser. E. Schweizerbart, Stuttgart. Utermo¨hl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplanktonmethodik. Mitt. Int. Verh. Limnol. 9, 1–38. Wagner, G.M., Mshigeni, K.E., 1986. The Utricularia–Cyanophyta association and its nitrogen-fixing capacity. Hydrobiologia 141, 255–261. Wallace, L.R., 1977. Substrate discrimination by larvae of the sessile rotifer Ptygura beauchampi Edmondson. Freshwater Biol. 7, 301–309.