With a Flick of the Lid: A Novel Trapping Mechanism in Nepenthes gracilis Pitcher Plants

Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
PLoS ONE (Impact Factor: 3.23). 06/2012; 7(6):e38951. DOI: 10.1371/journal.pone.0038951
Source: PubMed


Carnivorous pitcher plants capture prey with modified leaves (pitchers), using diverse mechanisms such as 'insect aquaplaning' on the wet pitcher rim, slippery wax crystals on the inner pitcher wall, and viscoelastic retentive fluids. Here we describe a new trapping mechanism for Nepenthes gracilis which has evolved a unique, semi-slippery wax crystal surface on the underside of the pitcher lid and utilises the impact of rain drops to 'flick' insects into the trap. Depending on the experimental conditions (simulated 'rain', wet after 'rain', or dry), insects were captured mainly by the lid, the peristome, or the inner pitcher wall, respectively. The application of an anti-slip coating to the lower lid surface reduced prey capture in the field. Compared to sympatric N. rafflesiana, N. gracilis pitchers secreted more nectar under the lid and less on the peristome, thereby directing prey mainly towards the lid. The direct contribution to prey capture represents a novel function of the pitcher lid.

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Available from: Bruno Di Giusto, Sep 29, 2015
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    • "The lid of Nepenthes pitchers is known to minimise rainwater entry into the pitcher (Bauer et al., 2012). Incoming water would not only threaten the bats but also dilute the digestive fluid and decrease the pitcher's digestive capabilities (Clarke, 2006). "
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    ABSTRACT: Whether mutualisms persist or vanish during the course of evolution depends on the cost-benefit ratio for the species involved. In the interaction between the pitcher plant Nepenthes hemsleyana and the bat Kerivoula hardwickii both partners mutually benefit: N. hemsleyana offers high quality roosts in exchange for nutrients from the bats’ faeces. Here, we tested the hypothesis that the partners should also incur costs from their interaction. In the field, we examined potential costs that are likely to occur in our system and that are already known to be present in other bat-plant interactions. Regarding the plants, the bats could injure the tissue of the fragile pitchers and thus affect the pitchers’ longevity. Regarding the bats, the ephemeral nature of N. hemsleyana pitchers and incoming rainwater could force them to switch these roosts more frequently than if using an alternative roost type. Our results suggest that neither the pitcher plants nor the bats accrue substantial costs from their interaction. We conclude that the ratio of high benefits to low costs strengthens this mutualism and promotes reciprocal adaptations and specialisations.
    Zoologischer Anzeiger - A Journal of Comparative Zoology 09/2015; 258:1-5. DOI:10.1016/j.jcz.2015.06.002 · 1.48 Impact Factor
    • "Nepenthes rafflesiana secreted the highest quantity of sugar, and N. ampullaria and N. gracilis the lowest (Figure 6). Nepenthes gracilis also secretes nectar onto the peristome (see Bauer et al. (2012) for a comparison of nectar secretion on the peristome and under the lid) but allocates a large proportion of its nectar secretion to the underside of the pitcher lid. Particularly in the early morning, large droplets of accumulated nectar can be found under N. gracilis lids (Figure 7 "
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    ABSTRACT: Carnivorous pitcher plants capture insect prey to acquire essential nutrients while growing on extremely poor soils. A few individual species have evolved mutualistic relationships with small mammals that visit the traps to harvest nectar, and in return leave faecal droppings in the pitchers. Here we report that a diverse guild of nectar-harvesting vertebrates visits pitchers of two common lowland Nepenthes species without providing any obvious benefit for the plants. Over four consecutive field seasons, we observed four species of sunbirds and one species of tree shrew drinking nectar from pitcher plants. Foraging activity was highest in the morning and late afternoon. Van Hasselt’s, Brown-throated and olive-backed sunbirds were regular and highly abundant pitcher visitors in two different field sites. A crimson sunbird and a lesser tree shrew were each observed harvesting nectar on one occasion. The vertebrates harvested nectar from the pitcher rim (peristome) of N. rafflesiana and from the underside of the pitcher lid of N. gracilis. A comparison of the nectar production of these and three further sympatric species revealed exceptionally high quantities of nectar for N. rafflesiana. Other factors such as plant and pitcher abundance and the habitat preferences of the observed vertebrates are likely to also play a role in their choice to visit particular species. This is the first account of a case of obvious nectar robbing from Nepenthes pitchers by a guild of species that are too large to serve as prey, while the pitcher size and shape prevent faecal droppings from reaching the pitcher’s inside. This interaction provides an example of a possible starting point for the evolution of the elaborate mutualistic relationships observed in some species. Follow-up adaptations of pitcher shape could enable the plants to catch the droppings of their visitors and turn an exploitative relationship into a mutualism.
    Journal of Natural History 01/2015; DOI:10.1080/00222933.2015.1059963 · 0.88 Impact Factor
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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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