Advances in Carnivorous Plants Research

Plants which catch and digest animals for their nutrition are called carnivorous (Latin: Carnis - flesh; Vorare - devour or swallow). Carnivorous plants share many features with non-carnivorous plants but possess a number of unique characters which have evolved as particular adaptations towards carnivory. The fact that certain plants are carnivorous was for a long time strictly denied (e.g., by Carl von Linné), and it was Charles [Darwin (1875)] who paved the way for its acceptance. Among the angiosperms carnivory has evolved independently several times and ca. 630 species are known to be carnivorous. In being botanical curiosities carnivorous plants have attracted considerable interest from both researchers and gardeners. Several comprehensive treatments (e.g., [Barthlott et al., 2004]) are available which provide insights into various aspects of this plant group. The last comprehensive monograph focusing on the physiology of carnivorous plants was published by [Juniper et al. in 1989]. Over the last decade the scientific interest in carnivorous plants increased resulting in numerous contributions about their phylogeny, ecology, and physiology, starting with a monumental monograph on Utricularia by Peter [Taylor (1989)]. Also floristic surveys of several regions were published (e.g., [Clarke, 1997]; [Lowrie, 1987], [1989], [1998]; [Salmon, 2001]; [Schnell, 2002]). Based on this growing interest the editors of this issue of Plant Biology decided to organize a symposium devoted to bring together those who are currently working with carnivorous plants. The symposium was held on the occasion of the XVII International Botanical Congress in Vienna in July 2005. This issue of Plant Biology summarizes selected contributions and gives an overview on current advances in research on carnivorous plants.

Almost all carnivorous plants grow in open habitats such as bogs, fens, rock outcrops, lakes, and ponds wherever light and moisture are abundant but macronutrients, especially nitrogen, phosphorus, and potassium are rare. Usually carnivory is interpreted as an adaptive trait in environments where relevant nutrients are scarce and light is not limiting. The cost-benefit model ([Givnish et al., 1984]) for the evolution of carnivorous plants postulates a trade-off between photosynthetic costs of carnivorous structures and photosynthetic benefits accrued through additional nutrient acquisition. Based on this model it can be predicted that carnivorous plants have an energetic advantage over non-carnivorous plants when nutrients are scarce but neither light nor water is limiting. In his review [Ellison (2006)] surveys published data on photosynthesis and nutrient limitation in carnivorous and non-carnivorous plants to test predictions of the cost-benefit model. He concludes that carnivorous plants are at an energetic disadvantage compared to non-carnivorous plants in similar habitats due to, e.g., a lower efficiency of photosynthetic nutrient use. Instead of being an optimal solution to the lack of nutrients, carnivory of plants seems to include a limited set of responses constrained by both phylogenetic history and harsh environmental conditions.

[Laakkonen et al. (2006)] deal with the evolution of carnivorous plants and their photosynthetic costs and benefits in nutrient-poor habitats. Trapping structures that are often less or non-photosynthetic may stress carnivores in terms of carbon production. The cost-benefit model ([Givnish et al., 1984]) for the evolution of carnivorous plants claims that carnivory is advantageous via higher photosynthetic rates in moist, sunny habitats. It is, however, doubtful whether this assumption holds true for active trapping systems where energy is required for active ion transport processes. Respiratory rates in bladders of Utricularia can be two orders of magnitude greater than in leafy structures. Interestingly, the subunit I (COX I) of the cytochrome c oxidase (COX, a multi-subunit enzyme that catalyzes the respiratory reduction of oxygen to water) of Utricularia deviates structurally from other eukaryotes, Archaea and Bacteria. [Laakkonen et al. (2006)] postulate that electron transport and proton pumping are decoupled in this case. This would permit Utricularia to optimize power output during times of need.

Carnivorous plants face the problem of what proportion of their biomass can be invested in building and maintaining trapping structures. The contribution of [Adamec (2006)] deals with the energetic costs of carnivory in aquatic Utricularia species. In this case net photosynthetic rate and respiration in bladders and leaves/shoot segments were measured. The results obtained clearly show that bladders have a very low photosynthetic efficiency and thus require considerable maintenance costs.

Genome size varies enormously in angiosperms with Arabidopsis thaliana (157 Mbp, 1C value) being usually cited as having the smallest genome. With regard to the relationship between genome size, life-cycle, and reproductive mode there are different hypotheses. After providing a concise introduction into genome sizes of angiosperms, [Greilhuber et al. (2006)] report for the first time details about genome sizes in the carnivorous Lentibulariaceae. Measurements of genome size were made from Feulgen-stained material using DNA image densitometry. The results show that three taxa of Lentibulariaceae (Genlisea margaretae with 63 Mbp, G. aurea with 64 Mbp, and Utricularia gibba with 88 Mbp) have a significantly lower genome size than A. thaliana and form interesting models for understanding ways of genome miniaturization. In G. aurea the smallest mitotic anaphase chromatids have 2.1 Mbp and are thus of bacterial size. Ultrasmall genomes have not been found in Pinguicula, which is the sister group of the Genlisea-Utricularia clade ([Greilhuber et al., 2006]).

The Lentibulariaceae (bladderworts) are the largest family of carnivorous plants and comprise ca. 325 species in three genera which are clearly differentiated with regard to their trapping system (Genlisea, Pinguicula, and Utricularia; [Fischer et al., 2004]). In [Müller et al. (2006)], the progress in understanding the phylogeny and evolution of Lentibulariaceae is reviewed. Recent work of this working group which was based on the use of various molecular markers has established that Lentibulariaceae and their three genera are monophyletic with Pinguicula being sister to a Genlisea-Utricularia clade. However, the closest relatives within the Lamiales remain uncertain. Remarkably, the genera Genlisea and Utricularia exhibit substitutional rates that rank among the highest in angiosperms for the molecular markers (e.g., trnK) analyzed. Obviously, in both genera a highly unconventional molecular evolutionary mode is realized what is further underlined by the finding of extremely low genome sizes in these plants ([Greilhuber et al., 2006]).

Within the Lentibulariaceae, the genus Pinguicula (butterworts) shows the most primitive trapping system, consisting of mucilage-covered leaves with margins that can be enrolled. Based on morphological (in particular embryo structures) and molecular data (ITS1 and ITS2 of the nuclear ribosomal DNA) the phylogeny of this genus is discussed by [Degtjareva et al. (2006)]. Pinguicula encompasses species with two cotyledons while others have only one cotyledon what is probably unique among the Lamiales. There are still controversies as to whether monocotyly is the result of the loss of the second cotyledon or of the fusion between two cotyledons. The results indicate that cotyledon number and sporoderm structure were quite unstable in the evolution of Pinguicula. Moreover, the data obtained imply homoplasy in the cotyledon number.

Whereas the elaborated trapping mechanisms of carnivorous plants have attracted much attention, their reproductive biology has remained neglected. Based on field observations in the Indian Western Ghats, [Hobbhahn et al. (2006)] present data on the pollination biology of selected terrestrial Utricularia species. In the rainy season the rocky lateritic plateaus of the Western Ghats are covered by millions of individuals of several Utricularia species which show the phenomenon of mass-flowering. The flowers of the species studied (U. albocaerulea, U. purpurascens, U. reticulata) contained extremely small volumes of nectar with high sugar concentrations. Despite low pollen/ovule-ratios autonomous selfing seems to play no role. In all three species the spatial arrangement of the reproductive organs makes an insect vector necessary for pollen transfer within and between flowers. More than 50 species of pollinating insects (e.g., bees, butterflies, hawk moths) were observed despite very adverse weather conditions on the peak of the monsoon season.

By definition carnivorous plants trap and digest their prey ([Juniper et al., 1989]). Plants which trap prey but depend on assistance for digestion are known as protocarnivores. [Darnowski et al. (2006)] report that in Australian triggerplants (Stylidium spp.; Stylidiaceae) which often occur side by side with carnivorous species of Drosera and Byblis insects are trapped by mucilage-secreting glandular hairs on their inflorescences and floral parts. According to the authors protease activity could be found in the glandular region of triggerplants. These observations provide indications for protocarnivory in Stylidium what has not been reported yet.

[Płachno et al. (2006)] focus on the activity of phosphatases in digestive glands of selected carnivorous plants, especially Lentibulariaceae. In the majority of cases tested by fluorescence labelling, activity of phosphatases was detected. High activity of phosphatases was also found in glands of Byblis and Roridula which are usually considered as protocarnivores. Based on this observation [Płachno et al. (2006)] propose that both Byblis and Roridula should be treated as true carnivorous plants.

There is evidence that carnivorous plants are unambiguously polyphyletic and at least five independent origins can be hypothesized. Within the Caryophyllales s.l. carnivory evolved in the Droseraceae, Drosophyllaceae, Nepenthaceae, and part of the Dioncophyllaceae (Triphyophyllum). [Heubl et al. (2006)] review the phylogenetic relationships of carnivorous taxa among the Caryophyllales s.l. and discuss character evolution within this lineage. Comparative sequencing of matK, trnK, atpB, rbcL, and nuclear 18S rDNA revealed a clear division of the Caryophyllales s.l. in a “core” and a “non-core” group. The latter comprises Polygonaceae, Plumbaginaceae, Frankeniaceae, Tamaricaceae, and the above mentioned carnivorous families plus Ancistrocladaceae. Interestingly carnivory was lost secondarily in Dioncophyllaceae (except Triphyophyllum) and Ancistrocladaceae. [Heubl et al. (2006)] suggest that pitfall traps of Nepenthes and snap traps (Aldrovanda, Dionaea) were derived from a common ancestor with adhesive flypaper traps.

Nepenthaceae, the pitcher plants of the Old World tropics show a remarkable diversity in SE-Asia, especially on the islands of Borneo and Sumatra which are considered to be a secondary center of diversity for Nepenthes. [Meimberg and Heubl (2006)] investigated the peptide transporter Transferase 1 (PTR 1), to develop a phylogenetic marker that is based on a nuclear low copy gene in Nepenthes. While in parts congruent to the plastid trnK intron phylogeny, a higher divergence of some sequences in PTR 1 and in the previously reported, non cpDNA dataset indicates that remnants of an older species stock persisted east of Wallace's line and on the Sunda Shelf suggesting that plastid haplotypes existing today in the main distribution center of the Nepenthaceae could be descendants of more recently dispersed lineages that had been transmitted to an old species stock.

In the Paleotropical genus Nepenthes, leaves are modified into pitfall pitcher traps which consist of several structural and functional zones, differing in macro-morphology, surface microstructure, and function ([Juniper et al., 1989]). [Gorb and Gorb (2006)] focus on the physico-chemical properties of epidermal surfaces in different pitcher zones (lid, peristome, waxy slippery zone, and the digestive zone) in N. alata and their influence on insect adhesion. These properties may determine the interaction between animal feet and plant surface, especially during contact formation. Apart from the waxy slippery zone the different pitcher surfaces are considered to support strong adhesion forces based on capillary interaction. The waxy surface is almost unwettable and essentially decreases insect adhesion.

At their natural growth sites the vase-shaped leaves of the North American pitcher plant Sarracenia purpurea are colonized by a great variety of aquatic organisms (e.g., bacteria, protozoans, invertebrates; [Hegner, 1926]). Only little is known about the occurrence of microalgae in pitchers of S. purpurea. This species was deliberately introduced into parts of Europe and [Gebühr et al. (2006)] provide information from Saxony, Germany on the structure of algae coenoses in the pitchers. Primary colonizers were taxa from the orders Chlamydomonadales, Chlorococcales, and Ochromonadales. Filamentous green algae (Klebsormidiales) became more abundant in older pitchers. Biomass of algae was considerable and reached more than 80 % of the living biomass in the pitchers. Possibly nitrogen and phosphorus present in the algae biomass might be used by S. purpurea as an additional source of nutrients.

Obviously, the scientific interest in carnivorous plants is unbroken. Our symposium is a modest contribution to this interest. The organization of the above mentioned symposium on carnivorous plants on the occasion of the XVII International Botanical Congress in Vienna in July 2005 and the publication of this special issue of Plant Biology is the result of support from the DFG (German Research Foundation) to the editors of this issue. Moreover, we gratefully acknowledge the help of Dr. Inge Theisen (Koblenz).

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