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Concept: Pitcher plant

170

Trade-offs among species' ecological interactions is a pervasive explanation for species coexistence. The traits associated with trade-offs are typically measured to mechanistically explain species coexistence at a single spatial scale. However, species potentially interact at multiple scales and this may be reflected in the traits among coexisting species. I quantified species' ecological traits associated with the trade-offs expected at both local (competitive ability and predator tolerance) and regional (competitive ability and colonization rate) community scales. The most common species (four protozoa and a rotifer) from the middle trophic level of a pitcher plant (Sarracenia purpurea) inquiline community were used to link species traits to previously observed patterns of species diversity and abundance. Traits associated with trade-offs (competitive ability, predator tolerance, and colonization rate) and other ecological traits (size, growth rate, and carrying capacity) were measured for each of the focal species. Traits were correlated with one another with a negative relationship indicative of a trade-off. Protozoan and rotifer species exhibited a negative relationship between competitive ability and predator tolerance, indicative of coexistence at the local community scale. There was no relationship between competitive ability and colonization rate. Size, growth rate, and carrying capacity were correlated with each other and the trade-off traits: Size was related to both competitive ability and predator tolerance, but growth rate and carrying capacity were correlated with predator tolerance. When partial correlations were conducted controlling for size, growth rate and carrying capacity, the trade-offs largely disappeared. These results imply that body size is the trait that provides the basis for ecological interactions and trade-offs. Altogether, this study showed that the examination of species' traits in the context of coexistence at different scales can contribute to our understanding of the mechanisms underlying community structure.

Concepts: Biodiversity, Ecology, Pitcher plant, Trophic level, Trophic dynamics, Carrying capacity, Sarracenia purpurea, Sarracenia

168

BACKGROUND: The purple pitcher plant, Sarracenia purpurea L., is a widely distributed species in North America with a history of use as both a marketed pain therapy and a traditional medicine in many aboriginal communities. Among the Cree of Eeyou Istchee in northern Quebec, the plant is employed to treat symptoms of diabetes and the leaf extract demonstrates multiple anti-diabetic activities including cytoprotection in an in vitro model of diabetic neuropathy. The current study aimed to further investigate this activity by identifying the plant parts and secondary metabolites that contribute to these cytoprotective effects. METHODS: Ethanolic extracts of S. purpurea leaves and roots were separately administered to PC12 cells exposed to glucose toxicity with subsequent assessment by two cell viability assays. Assay-guided fractionation of the active extract and fractions was then conducted to identify active principles. Using high pressure liquid chromatography together with mass spectrometry, the presence of identified actives in both leaf and root extracts were determined. RESULTS: The leaf extract, but not that of the root, prevented glucose-mediated cell loss in a concentration-dependent manner. Several fractions elicited protective effects, indicative of multiple active metabolites, and, following subfractionation of the polar fraction, hyperoside (quercetin-3-O-galactoside) and morroniside were isolated as active constituents. Phytochemical analysis confirmed the presence of hyperoside in the leaf but not root extract and, although morroniside was detected in both organs, its concentration was seven times higher in the leaf. CONCLUSION: Our results not only support further study into the therapeutic potential and safety of S. purpurea as an alternative and complementary treatment for diabetic complications associated with glucose toxicity but also identify active principles that can be used for purposes of standardization and quality control.

Concepts: Nutrition, Diabetes mellitus, Cell culture, Pitcher plant, Sarracenia purpurea, Sarracenia, Sarraceniaceae, Sarracenia rosea

65

Carnivorous Nepenthes pitcher plants capture arthropods with specialized slippery surfaces. The key trapping surface, the pitcher rim (peristome), is highly slippery when wetted by rain, nectar or condensation, but not when dry. As natural selection should favour adaptations that maximize prey intake, the evolution of temporarily inactive traps seems paradoxical. Here, we show that intermittent trap deactivation promotes ‘batch captures’ of ants. Prey surveys revealed that N. rafflesiana pitchers sporadically capture large numbers of ants from the same species. Continuous experimental wetting of the peristome increased the number of non-recruiting prey, but decreased the number of captured ants and shifted their trapping mode from batch to individual capture events. Ant recruitment was also lower to continuously wetted pitchers. Our experimental data fit a simple model that predicts that intermittent, wetness-based trap activation should allow safe access for ‘scout’ ants under dry conditions, thereby promoting recruitment and ultimately higher prey numbers. The peristome trapping mechanism may therefore represent an adaptation for capturing ants. The relatively rare batch capture events may particularly benefit larger plants with many pitchers. This explains why young plants of many Nepenthes species additionally employ wetness-independent, waxy trapping surfaces.

Concepts: Natural selection, Evolution, Species, Carnivorous plant, Pitcher plant, Cretaceous, Charles Darwin, Nepenthes

46

Plants use rapid movements to disperse seed, spores, or pollen and catch animal prey. Most rapid-release mechanisms only work once and, if repeatable, regaining the prerelease state is a slow and costly process. We present an encompassing mechanism for a rapid, repeatable, passive-dynamic motion used by a carnivorous pitcher plant to catch prey. Nepenthes gracilis uses the impact of rain drops to catapult insects from the underside of the canopy-like pitcher lid into the fluid-filled trap below. High-speed video and laser vibrometry revealed that the lid acts as a torsional spring system, driven by rain drops. During the initial downstroke, the tip of the lid reached peak velocities similar to fast animal motions and an order of magnitude faster than the snap traps of Venus flytraps and catapulting tentacles of the sundew Drosera glanduligera. In contrast to these active movements, the N. gracilis lid oscillation requires neither mechanical preloading nor metabolic energy, and its repeatability is only limited by the intensity and duration of rainfall. The underside of the lid is coated with friction-reducing wax crystals, making insects more vulnerable to perturbations. We show that the trapping success of N. gracilis relies on the combination of material stiffness adapted for momentum transfer and the antiadhesive properties of the wax crystal surface. The impact-driven oscillation of the N. gracilis lid represents a new kind of rapid plant movement with adaptive function. Our findings establish the existence of a continuum between active and passive trapping mechanisms in carnivorous plants.

Concepts: Plant, Animal, Carnivorous plant, Pitcher plant, Rapid plant movement, Drosera, Droseraceae, Venus Flytrap

38

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.

Concepts: Plant, Predation, Animal, Nutrient, Carnivorous plant, Pitcher plant, Ant, Herbivore

28

Slow changes in underlying state variables can lead to “tipping points,” rapid transitions between alternative states (“regime shifts”) in a wide range of complex systems. Tipping points and regime shifts routinely are documented retrospectively in long time series of observational data. Experimental induction of tipping points and regime shifts is rare, but could lead to new methods for detecting impending tipping points and forestalling regime shifts. By using controlled additions of detrital organic matter (dried, ground arthropod prey), we experimentally induced a shift from aerobic to anaerobic states in a miniature aquatic ecosystem: the self-contained pools that form in leaves of the carnivorous northern pitcher plant, Sarracenia purpurea. In unfed controls, the concentration of dissolved oxygen ([O2]) in all replicates exhibited regular diurnal cycles associated with daytime photosynthesis and nocturnal plant respiration. In low prey-addition treatments, the regular diurnal cycles of [O2] were disrupted, but a regime shift was not detected. In high prey-addition treatments, the variance of the [O2] time series increased until the system tipped from an aerobic to an anaerobic state. In these treatments, replicate [O2] time series predictably crossed a tipping point at ∼45 h as [O2] was decoupled from diurnal cycles of photosynthesis and respiration. Increasing organic-matter loading led to predictable changes in [O2] dynamics, with high loading consistently driving the system past a well-defined tipping point. The Sarracenia microecosystem functions as a tractable experimental system in which to explore the forecasting and management of tipping points and alternative regimes.

Concepts: Photosynthesis, Oxygen, Carbon dioxide, Cellular respiration, Pitcher plant, Sarracenia purpurea, Sarracenia, Sarraceniaceae

28

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.

Concepts: Photosynthesis, Insect, Matter, Animal, Carnivorous plant, Pitcher plant, Cretaceous, Nepenthes

20

Mutualisms between plants and animals shape the world’s ecosystems [1, 2]. In such interactions, achieving contact with the partner species is imperative. Plants regularly advertise themselves with signals that specifically appeal to the partner’s perceptual preferences [3-5]. For example, many plants have acquired traits such as brightly colored, fragrant flowers that attract pollinators with visual, olfactory, or-in the case of a few bat-pollinated flowers-even acoustic stimuli in the form of echo-reflecting structures [6-9]. However, acoustic attraction in plants is rare compared to other advertisements and has never been found outside the pollination context and only in the Neotropics. We hypothesized that this phenomenon is more widespread and more diverse as plant-bat interactions also occur in the Paleotropics. In Borneo, mutualistic bats fertilize a carnivorous pitcher plant while roosting in its pitchers [10, 11]. The pitcher’s orifice features a prolonged concave structure, which we predicted to distinctively reflect the bats' echolocation calls for a wide range of angles. This structure should facilitate the location and identification of pitchers even within highly cluttered surroundings. Pitchers lacking this structure should be less attractive for the bats. Ensonifications of the pitchers around their orifice revealed that this structure indeed acts as a multidirectional ultrasound reflector. In behavioral experiments where bats were confronted with differently modified pitchers, the reflector’s presence clearly facilitated the finding and identification of pitchers. These results suggest that plants have convergently acquired reflectors in the Paleotropics and the Neotropics to acoustically attract bats, albeit for completely different ecological reasons.

Concepts: Scientific method, Plant, Animal, Symbiosis, Ultrasound, Pollination, Carnivorous plant, Pitcher plant

4

Nepenthes pitcher plants display interspecific diversity in pitcher form and diets. This species-rich genus might be a conspicuous candidate for an adaptive radiation. However, the pitcher traits of different species have never been quantified in a comparative study, nor have their possible adaptations to the resources they exploit been tested. In this study, we compare the pitcher features and prey composition of the seven Nepenthes taxa that grow in the heath forest of Brunei (Borneo) and investigate whether these species display different trapping syndromes that target different prey. The Nepenthes species are shown to display species-specific combinations of pitcher shapes, volumes, rewards, attraction and capture traits, and different degrees of ontogenetic pitcher dimorphism. The prey spectra also differ among plant species and between ontogenetic morphotypes in their combinations of ants, flying insects, termites, and noninsect guilds. According to a discriminant analysis, the Nepenthes species collected at the same site differ significantly in prey abundance and composition at the level of order, showing niche segregation but with varying degrees of niche overlap according to pairwise species comparisons. Weakly carnivorous species are first characterized by an absence of attractive traits. Generalist carnivorous species have a sweet odor, a wide pitcher aperture, and an acidic pitcher fluid. Guild specializations are explained by different combinations of morpho-functional traits. Ant captures increase with extrafloral nectar, fluid acidity, and slippery waxy walls. Termite captures increase with narrowness of pitchers, presence of a rim of edible trichomes, and symbiotic association with ants. The abundance of flying insects is primarily correlated with pitcher conicity, pitcher aperture diameter, and odor presence. Such species-specific syndromes favoring resource partitioning may result from local character displacement by competition and/or previous adaptations to geographically distinct environments.

Concepts: Evolution, Insect, Plant, Ecology, Pitcher plant, Ant, Nepenthes, Termite

1

Numerous natural systems contain surfaces or threads that enable directional water transport. This behaviour is usually ascribed to hierarchical structural features at the microscale and nanoscale, with gradients in surface energy and gradients in Laplace pressure thought to be the main driving forces. Here we study the prey-trapping pitcher organs of the carnivorous plant Nepenthes alata. We find that continuous, directional water transport occurs on the surface of the ‘peristome’-the rim of the pitcher-because of its multiscale structure, which optimizes and enhances capillary rise in the transport direction, and prevents backflow by pinning in place any water front that is moving in the reverse direction. This results not only in unidirectional flow despite the absence of any surface-energy gradient, but also in a transport speed that is much higher than previously thought. We anticipate that the basic ‘design’ principles underlying this behaviour could be used to develop artificial fluid-transport systems with practical applications.

Concepts: Human, Plant, Structure, Vector field, Surface tension, System, Carnivorous plant, Pitcher plant