Mass March of termites into the deadly trap

Fachbereich Biologie, Zoologisches Institut, Johann Wolfgang Goethe-Universität, Frankfurt am Main, Postfach 111932, 60054 Frankfurt, Germany.
Nature (Impact Factor: 41.46). 01/2002; 415(6867):36-37. DOI: 10.1038/415036a


Carnivorous pitcher plants of the genus Nepenthes are not usually very selective about their prey, catching anything that is careless enough to walk on their slippery peristome, but Nepenthes albomarginata is an exception. We show here that this plant uses a fringe of edible white hairs to lure and then trap its prey, which consists exclusively of termites in enormous numbers. This singular feature accounts for the specialization of N. albomarginata for one prey taxon, unique so far among carnivorous plants.

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    • "It is likely that the nutritional benefits more than compensate the costs that N. bicalcarata might incur for housing the ants, such as the possible nutrient export via winged males and queens of C. schmitzi itself, the production of hollow tendril domatia and an increased nectar secretion [18]. Our study adds to a growing body of evidence showing that many alternative nutrient acquisition strategies have evolved in the genus Nepenthes [27], [37], [49]–[54]. "
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    ABSTRACT: Many plants combat herbivore and pathogen attack indirectly by attracting predators of their herbivores. Here we describe a novel type of insect-plant interaction where a carnivorous plant uses such an indirect defence to prevent nutrient loss to kleptoparasites. The ant Camponotus schmitzi is an obligate inhabitant of the carnivorous pitcher plant Nepenthes bicalcarata in Borneo. It has recently been suggested that this ant-plant interaction is a nutritional mutualism, but the detailed mechanisms and the origin of the ant-derived nutrient supply have remained unexplained. We confirm that N. bicalcarata host plant leaves naturally have an elevated (15)N/(14)N stable isotope abundance ratio (δ(15)N) when colonised by C. schmitzi. This indicates that a higher proportion of the plants' nitrogen is insect-derived when C. schmitzi ants are present (ca. 100%, vs. 77% in uncolonised plants) and that more nitrogen is available to them. We demonstrated direct flux of nutrients from the ants to the host plant in a (15)N pulse-chase experiment. As C. schmitzi ants only feed on nectar and pitcher contents of their host, the elevated foliar δ(15)N cannot be explained by classic ant-feeding (myrmecotrophy) but must originate from a higher efficiency of the pitcher traps. We discovered that C. schmitzi ants not only increase the pitchers' capture efficiency by keeping the pitchers' trapping surfaces clean, but they also reduce nutrient loss from the pitchers by predating dipteran pitcher inhabitants (infauna). Consequently, nutrients the pitchers would have otherwise lost via emerging flies become available as ant colony waste. The plants' prey is therefore conserved by the ants. The interaction between C. schmitzi, N. bicalcarata and dipteran pitcher infauna represents a new type of mutualism where animals mitigate the damage by nutrient thieves to a plant.
    PLoS ONE 05/2013; 8(5):e63556. DOI:10.1371/journal.pone.0063556 · 3.23 Impact Factor
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    • "The compact anatomy of traps (reminiscent of roots), which is to restrict apoplastic conductivity (Pavlovič et al., 2007), serves the selective symplastic transport of nutrients gained from carnivory. Investments in the following cause considerable maintenance costs: attractants such as nectars and odours (Juniper et al., 1989; Moran, 1996; Bohn and Federle, 2004; Bennett and Ellison, 2009; Bhattarai and Horner, 2009; Jürgens et al., 2009); edible trichomes (Merbach et al., 2002); colourful projections (Schaefer and Ruxton, 2008) and UV patterns (Moran et al., 1999); resinous droplets (Voigt and Gorb, 2010) or slime that in Drosophyllum has a scent of honey, which may mimic nectar (Jürgens et al., 2009); glands excreting mucilage (Drosera, Pinguicula, Byblis) or a hydrophobic resin (Roridula) to catch prey (Juniper et al., 1989); glands excreting digestive enzymes – these digestive glands, with their attendant mechanisms for simultaneous enzyme secretion and nutrient absorption are an anatomical birthmark of the carnivorous syndrome (Lüttge, 1971; Benzing et al., 1976); exudation of organic compounds to support the microbial community associated with the traps (Sirová et al., 2009, 2010); and nutrient uptake machinery (An et al., 2001) required for functioning of each single trap (Knight, 1992; Adamec, 2006, 2010a; Pavlovič et al., 2007; Hájek and Adamec, 2010). Therefore, it is not surprising that the dual use of leaves for photosynthesis and nutrient uptake has deeply reduced the net photosynthetic rate of terrestrial carnivorous plants, leading ultimately to reduction of the relative growth rate (Ellison, 2006; Farnsworth and Ellison, 2008); giant carnivorous species are the exception rather than the rule: Triphyophyllum peltatum, Nepenthes rajah, N. edwardsi ana, N. ampullaria, N. rafflesiana and N. rafflesiana var. "
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    ABSTRACT: A plant is considered carnivorous if it receives any noticeable benefit from catching small animals. The morphological and physiological adaptations to carnivorous existence is most complex in plants, thanks to which carnivorous plants have been cited by Darwin as 'the most wonderful plants in the world'. When considering the range of these adaptations, one realizes that the carnivory is a result of a multitude of different features. This review discusses a selection of relevant articles, culled from a wide array of research topics on plant carnivory, and focuses in particular on physiological processes associated with active trapping and digestion of prey. Carnivory offers the plants special advantages in habitats where nutrient supply is scarce. Counterbalancing costs are the investments in synthesis and the maintenance of trapping organs and hydrolysing enzymes. With the progress in genetic, molecular and microscopic techniques, we are well on the way to a full appreciation of various aspects of plant carnivory. Sufficiently complex to be of scientific interest and finite enough to allow conclusive appraisal, carnivorous plants can be viewed as unique models for the examination of rapid organ movements, plant excitability, enzyme secretion, nutrient absorption, food-web relationships, phylogenetic and intergeneric relationships or structural and mineral investment in carnivory.
    Annals of Botany 09/2011; 109(1):47-64. DOI:10.1093/aob/mcr249 · 3.65 Impact Factor
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    • "Prey capture and digestion through pitchers in these plants are primarily an adaptation to live in low nutrient soils (Bohn and Federle, 2004; Hatano and Hamada, 2008; Bauer et al., 2011). Insects, spiders, ants, termites, snails, and other small organisms are attracted or drawn by chance encounters into these biological prey traps (Merbach et al., 2002; Ellison and Gotelli, 2009). "
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    ABSTRACT: Prey capture and digestion in Nepenthes spp. through their leaf-evolved biological traps involve a sequence of exciting events. Sugar-rich nectar, aroma chemicals, narcotic alkaloid secretions, slippery wax crystals, and other biochemicals take part in attracting, capturing, and digesting preys in Nepenthes pitchers. Here we report the distribution of three potent naphthoquinones in Nepenthes khasiana and their roles in prey capture. Plumbagin was first detected in N. khasiana, and its content (root: 1.33 ± 0.02%, dry wt.) was the highest found in any natural source. Chitin induction enhanced plumbagin levels in N. khasiana (root: 2.17 ± 0.02%, dry wt.). Potted N. khasiana plants with limited growth of roots and aerial parts, showed higher levels of plumbagin accumulation (root: 1.92 ± 0.02%; root, chitin induction: 3.30 ± 0.21%, dry wt.) compared with field plants. Plumbagin, a known toxin, insect ecdysis inhibitor, and antimicrobial, was also found embedded in the waxy layers at the top prey capture region of N. khasiana pitchers. Chitin induction, mimicking prey capture, produced droserone and 5-O-methyl droserone in N. khasiana pitcher fluid. Both these naphthoquinone derivatives provide antimicrobial protection to the pitcher fluid from visiting preys. A two-way barrier was found between plumbagin and its two derivatives. Plumbagin was never detected in the pitcher fluid whereas both its derivatives were only found in the pitcher fluid on chitin induction or prey capture. The three naphthoquinones, plumbagin, droserone, and 5-O-methyl droserone, act as molecular triggers in prey capture and digestion in the carnivorous plant, N. khasiana.
    Journal of Experimental Botany 08/2011; 62(15):5429-36. DOI:10.1093/jxb/err219 · 5.53 Impact Factor
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