Abstract
Some 450 species of insectivorous plants have been discovered since Darwin published his work on the subject in 18751. We report here the first known case of a plant that traps and digests protozoa.
Main
Insectivorous plants colonize nutrient-poor places, and their major source of phosphorus, nitrogen and other elements is trapped and digested insects2,3. Extravagant trap-like structures are seen in the genus Genlisea (a member of the Lentibulariaceae, with the carnivorous genera Pinguicula and Utricularia) which occurs mainly in nutrient-poor white sands and moist rock outcrops in South America and tropical Africa. However, proof of the plant's carnivorous nature was previously lacking.
Genlisea species are rare in the wild and difficult to cultivate. Most form a small rosette about three centimetres in diameter, close to the ground, with linear or spatulate leaves. The yellow or violet flowers, similar to those of the related Antirrhinum, are borne on an inflorescence some 20 cm high.
When the rosette of Genlisea is dug up, pale bundles of root-like organs up to 15 cm long are revealed (Fig. 1a). However, the plant is rootless and these organs are subterranean leaves, highly modified and lacking chlorophyll4,5,6. The long, solid, basal part of the leaf attached to the rhizome opens into a hollow utricle. This contracts into a narrow tubular channel (the ‘neck piece’) which divides into two arms at an angle of 90-130° so that the apical part of the leaf is shaped like an inverted letter ‘Y’. The helically contorted arms are hollow, with an average inside diameter of 200 micrometres. The arms bear slit-like openings (width 400 μm, height 180 μm) lined with rows of hairs pointing towards the utricle, and numerous glands.
Since Darwin's time, it has been postulated that these specialized leaves are traps for catching prey, but there has been no proof of carnivory. Arthropod remnants have only exceptionally been found in the traps. This, and the dimensions of the traps, suggested to us that the subterranean leaves might function as highly specialized traps for catching protozoa.
To test this idea, we cultivated species of Genlisea in a greenhouse. Laboratory experiments were conducted with G. aurea, G. violacea and G. margaretae. Intact plants were placed in a Petri dish and ciliates such as Blepharisma americana were added.
The root-like subterranean organs of Genlisea proved attractive to protozoa (Fig. 1b). A few minutes after starting the experiment, numerous protozoa had already entered the traps (Fig. 1c). In contrast, living roots from plants occurring in the same habitats — such as Eriocaulon plumale — failed to attract ciliates.
The presence of acid phosphatases and esterases in G. africana7 suggests that the ciliates are digested. Additional experiments proved the existence of an attractant and indicated that Genlisea attracts protozoa chemotactically, trapping them in its subterranean leaves.
Genlisea can therefore be regarded as a highly specialized protozoan trap. Experiments using ciliates marked with the isotope sulphur-35 demonstrated its uptake by the trap leaves of Genlisea. After two days, 35S was traceable in the rosette leaves.
Field investigations at a natural site in the northern part of the Ivory Coast in west Africa indicate that, at this site at least, nine different ciliate species, as well as other protozoa, are trapped in large amounts by G. stapfii. Thus, 125 years after Charles Darwin's initial postulations, the puzzle of Genlisea's feeding habits seems to have been solved.
References
Darwin, C. Insectivorous Plants (Murray, London, 1875).
Juniper, B. E., Robins, R. J. &Joel, D. M. The Carnivorous Plants (Academic, London, 1989).
Lloyd, F. E. The Carnivorous Plants (Chronica Botanica, Waltham, 1942).
Goebel, K. Organographie der Pflanzen part 1, 3rd edn (Fischer, Jena, 1928).
Warming, E. Medd. Kjøb. 1, 33–70 (1874).
Reut, M. S. Bot. Helv. 103, 101-111 (1993).
Hop-Harrison, Y. in Lysosomes in Biology and Pathology 4 (eds Dingle, J. T. &Dean, R. T.) 525-578 (North Holland, Amsterdam, 1975).
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Barthlott, W., Porembski, S., Fischer, E. et al. First protozoa-trapping plant found. Nature 392, 447 (1998). https://doi.org/10.1038/33037
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DOI: https://doi.org/10.1038/33037
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