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How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

ABSTRACT: 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.

SUBMITTER: Bauer U

PROVIDER: S-EPMC4309005 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

Bauer Ulrike U Federle Walter W Seidel Hannes H Grafe T Ulmar TU Ioannou Christos C CC

Proceedings. Biological sciences 20150201 1801

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 pitcher ...[more]

PMID: 25589604

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Project description:BackgroundCarnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs.PitcherFluid as a Habitat The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O(2) and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water.InquilineDiversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. MUTUALISTIC: Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N(2).ConclusionsThere is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.

Project description:BackgroundThe leaves of carnivorous pitcher plants harbor diverse communities of inquiline species, including bacteria and larvae of the pitcher plant mosquito (Wyeomyia smithii), which aid the plant by processing captured prey. Despite the growing appreciation for this microecosystem as a tractable model in which to study food web dynamics and the moniker of W. smithii as a 'keystone predator', very little is known about microbiota acquisition and assembly in W. smithii mosquitoes or the impacts of W. smithii-microbiota interactions on mosquito and/or plant fitness.ResultsIn this study, we used high throughput sequencing of bacterial 16S rRNA gene amplicons to characterize and compare microbiota diversity in field- and laboratory-derived W. smithii larvae. We then conducted controlled experiments in the laboratory to better understand the factors shaping microbiota acquisition and persistence across the W. smithii life cycle. Methods were also developed to produce axenic (microbiota-free) W. smithii larvae that can be selectively recolonized with one or more known bacterial species in order to study microbiota function. Our results support a dominant role for the pitcher environment in shaping microbiota diversity in W. smithii larvae, while also indicating that pitcher-associated microbiota can persist in and be dispersed by adult W. smithii mosquitoes. We also demonstrate the successful generation of axenic W. smithii larvae and report variable fitness outcomes in gnotobiotic larvae monocolonized by individual bacterial isolates derived from naturally occurring pitchers in the field.ConclusionsThis study provides the first information on microbiota acquisition and assembly in W. smithii mosquitoes. This study also provides the first evidence for successful microbiota manipulation in this species. Altogether, our results highlight the value of such methods for studying host-microbiota interactions and lay the foundation for future studies to understand how W. smithii-microbiota interactions shape the structure and stability of this important model ecosystem.

Dataset Information

How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

Publications

How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants.

Similar Datasets

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