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      Where Is My Food? Brazilian Flower Fly Steals Prey from Carnivorous Sundews in a Newly Discovered Plant-Animal Interaction

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          Abstract

          A new interaction between insects and carnivorous plants is reported from Brazil. Larvae of the predatory flower fly Toxomerus basalis (Diptera: Syrphidae: Syrphinae) have been found scavenging on the sticky leaves of several carnivorous sundew species ( Drosera, Droseraceae) in Minas Gerais and São Paulo states, SE Brazil. This syrphid apparently spends its whole larval stage feeding on prey trapped by Drosera leaves. The nature of this plant-animal relationship is discussed, as well as the Drosera species involved, and locations where T. basalis was observed. 180 years after the discovery of this flower fly species, its biology now has been revealed. This is (1) the first record of kleptoparasitism in the Syrphidae, (2) a new larval feeding mode for this family, and (3) the first report of a dipteran that shows a kleptoparasitic relationship with a carnivorous plant with adhesive flypaper traps. The first descriptions of the third instar larva and puparium of T. basalis based on Scanning Electron Microscope analysis are provided.

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          Energetics and the evolution of carnivorous plants--Darwin's 'most wonderful plants in the world'.

          Carnivory has evolved independently at least six times in five angiosperm orders. In spite of these independent origins, there is a remarkable morphological convergence of carnivorous plant traps and physiological convergence of mechanisms for digesting and assimilating prey. These convergent traits have made carnivorous plants model systems for addressing questions in plant molecular genetics, physiology, and evolutionary ecology. New data show that carnivorous plant genera with morphologically complex traps have higher relative rates of gene substitutions than do those with simple sticky traps. This observation suggests two alternative mechanisms for the evolution and diversification of carnivorous plant lineages. The 'energetics hypothesis' posits rapid morphological evolution resulting from a few changes in regulatory genes responsible for meeting the high energetic demands of active traps. The 'predictable prey capture hypothesis' further posits that complex traps yield more predictable and frequent prey captures. To evaluate these hypotheses, available data on the tempo and mode of carnivorous plant evolution were reviewed; patterns of prey capture by carnivorous plants were analysed; and the energetic costs and benefits of botanical carnivory were re-evaluated. Collectively, the data are more supportive of the energetics hypothesis than the predictable prey capture hypothesis. The energetics hypothesis is consistent with a phenomenological cost-benefit model for the evolution of botanical carnivory, and also accounts for data suggesting that carnivorous plants have leaf construction costs and scaling relationships among leaf traits that are substantially different from those of non-carnivorous plants.
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            A Viscoelastic Deadly Fluid in Carnivorous Pitcher Plants

            Background The carnivorous plants of the genus Nepenthes, widely distributed in the Asian tropics, rely mostly on nutrients derived from arthropods trapped in their pitcher-shaped leaves and digested by their enzymatic fluid. The genus exhibits a great diversity of prey and pitcher forms and its mechanism of trapping has long intrigued scientists. The slippery inner surfaces of the pitchers, which can be waxy or highly wettable, have so far been considered as the key trapping devices. However, the occurrence of species lacking such epidermal specializations but still effective at trapping insects suggests the possible implication of other mechanisms. Methodology/Principal Findings Using a combination of insect bioassays, high-speed video and rheological measurements, we show that the digestive fluid of Nepenthes rafflesiana is highly viscoelastic and that this physical property is crucial for the retention of insects in its traps. Trapping efficiency is shown to remain strong even when the fluid is highly diluted by water, as long as the elastic relaxation time of the fluid is higher than the typical time scale of insect movements. Conclusions/Significance This finding challenges the common classification of Nepenthes pitchers as simple passive traps and is of great adaptive significance for these tropical plants, which are often submitted to high rainfalls and variations in fluid concentration. The viscoelastic trap constitutes a cryptic but potentially widespread adaptation of Nepenthes species and could be a homologous trait shared through common ancestry with the sundew (Drosera) flypaper plants. Such large production of a highly viscoelastic biopolymer fluid in permanent pools is nevertheless unique in the plant kingdom and suggests novel applications for pest control.
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              The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities.

              The ability of American carnivorous pitcher plants (Sarracenia) to digest insect prey is facilitated by microbial associations. Knowledge of the details surrounding this interaction has been limited by our capability to characterize bacterial diversity in this system. To describe microbial diversity within and between pitchers of one species, Sarracenia alata, and to explore how these communities change over time as pitchers accumulate and digest insect prey, we collected and analyzed environmental sequence tag (454 pyrosequencing) and genomic fingerprint (automated ribosomal intergenic spacer analysis and terminal restriction fragment length polymorphism) data. Microbial richness associated with pitcher plant fluid is high; more than 1,000 unique phylogroups were identified across at least seven phyla and 50 families. We documented an increase in bacterial diversity and abundance with time and observed repeated changes in bacterial community composition. Pitchers from different plants harbored significantly more similar bacterial communities at a given time point than communities coming from the same genetic host over time. The microbial communities in pitcher plant fluid also differ significantly from those present in the surrounding soil. These findings indicate that the bacteria associated with pitcher plant leaves are far from random assemblages and represent an important step toward understanding this unique plant-microbe interaction.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 May 2016
                2016
                : 11
                : 5
                : e0153900
                Affiliations
                [1 ]Botanische Staatssammlung München, Munich, Germany
                [2 ]GeoBio-Center LMU, Center of Geobiology and Biodiversity Research, Ludwig-Maximilians-University, Munich, Germany
                [3 ]Illumina, San Francisco, California, United States of America
                [4 ]Laboratório de Sistemática Vegetal, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil
                [5 ]Departamento de Ciencias Naturales y Recursos Naturales / Instituto CIBIO, Universidad de Alicante, Alicante, Spain
                [6 ]Zoologisches Forschungsmuseum Alexander Koenig, Leibniz-Institut für Biodiversität der Tiere, Bonn, Germany
                Natural Resources Canada, CANADA
                Author notes

                Competing Interests: Co-author FR is an employee of Illumina, a commercial company. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: AF FR XM. Performed the experiments: FR PMG CP-B XM. Analyzed the data: AF CP-B XM SR. Contributed reagents/materials/analysis tools: AF FR PMG CP-B XM SR. Wrote the paper: AF FR PMG CP-B XM SR.

                Author information
                http://orcid.org/0000-0002-4917-4736
                Article
                PONE-D-16-04224
                10.1371/journal.pone.0153900
                4856264
                27144980
                57be5ebe-1e52-48c5-814a-7ba8f86ea692
                © 2016 Fleischmann et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 February 2016
                : 5 April 2016
                Page count
                Figures: 2, Tables: 1, Pages: 15
                Funding
                Funded by: Illumina
                Award Recipient :
                The commercial funder Illumina provided support in the form of salaries for FR, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Larvae
                Biology and Life Sciences
                Organisms
                Plants
                Carnivorous Plants
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flowers
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Metamorphosis
                Pupae
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Insect Metamorphosis
                Pupae
                Physical Sciences
                Materials Science
                Materials by Attribute
                Adhesives
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Custom metadata
                DNA sequences have been deposited at the National Center for Biotechnology Information (NCBI) GenBank with the accession numbers KU216212 - KU216216.

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