in

Tropical pitcher plants (Nepenthes) act as ecological filters by altering properties of their fluid microenvironments

  • 1.

    George, L. O. & Bazzaz, F. The fern understory as an ecological filter: emergence and establishment of canopy-tree seedlings. Ecology 80, 833–845 (1999).

    • Article
    • Google Scholar
  • 2.

    Itô, H. & Hino, T. Dwarf bamboo as an ecological filter for forest regeneration. Ecological Research 22, 706–711 (2007).

    • Article
    • Google Scholar
  • 3.

    Tiitsaar, A., Kaasik, A. & Teder, T. The effects of seasonally variable dragonfly predation on butterfly assemblages. Ecology 94, 200–7 (2013).

  • 4.

    Muñoz, J. C. et al. Contribution of woody habitat islands to the conservation of birds and their potential ecosystem services in an extensive Colombian rangeland. Agriculture, Ecosystems &. Environment 173, 13–19 (2013).

    • Google Scholar
  • 5.

    Stagaman, K., Burns, A. R., Guillemin, K. & Bohannan, B. J. The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish. The ISME Journal 11, 1630 (2017).

  • 6.

    Krueger, L. M. & Peterson, C. J. Effects of woody debris and ferns on herb-layer vegetation and deer herbivory in a Pennsylvania forest blowdown. Ecoscience 16, 461–469 (2009).

    • Article
    • Google Scholar
  • 7.

    Bump, J. K. et al. Ungulate carcasses perforate ecological filters and create biogeochemical hotspots in forest herbaceous layers allowing trees a competitive advantage. Ecosystems 12, 996–1007 (2009).

    • Article
    • Google Scholar
  • 8.

    Duflot, R., Georges, R., Ernoult, A., Aviron, S. & Burel, F. Landscape heterogeneity as an ecological filter of species traits. Acta Oecologica 56, 19–26 (2014).

  • 9.

    Juniper, B. E., Robins, R. J. & Joel, D. M. The Carnivorous Plants. (London, etc.: Academic Press, 1989).

  • 10.

    Bittleston, L. S., Baker, C., Strominger, L. B., Pringle, A. & Pierce, N. E. Metabarcoding as a tool for investigating arthropod diversity in Nepenthes pitcher plants. Austral Ecology 41, 120–132 (2016).

    • Article
    • Google Scholar
  • 11.

    Fashing, N. J. Nepenthacarus, a new genus of Histiostomatidae (Acari: Astigmata) inhabiting the pitchers of Nepenthes mirabilis (Lour.) Druce in far north Queensland, Australia. Australian Journal of Entomology 41, 7–17 (2002).

    • Article
    • Google Scholar
  • 12.

    Kitching, R. A preliminary account of the metazoan food webs in phytotelmata from Sulawesi. Malay. Nat. J 41, 1–12 (1987).

    • Google Scholar
  • 13.

    Beaver, R. Biological studies of the fauna of pitcher plants [Nepenthes] in west Malaysia. in Annales de la Société Entomologique de France 15, 3–17 (1979).

  • 14.

    Ovaskainen, O. et al. How to make more out of community data? A conceptual framework and its implementation as models and software. Ecology Letters 20, 561–576 (2017).

  • 15.

    Kraft, N. J. et al. Community assembly, coexistence and the environmental filtering metaphor. Functional Ecology 29, 592–599 (2015).

    • Article
    • Google Scholar
  • 16.

    Lewontin, R. C. The Organism as the Subject and Object of Evolution. Scientia 118, 63–82 (1983).

    • Google Scholar
  • 17.

    Odling-Smee, F. Niche-constructing Phenotypes. (1988).

  • 18.

    Turner, J. The Extended Organism. The Physiology of Animal-Built Structures. (Cambridge: Harvard University Press, 2000).

  • 19.

    Turner, J. S. A superorganism’s fuzzy boundaries. Natural History 111, 62–69 (2002).

    • Google Scholar
  • 20.

    Dawkins, R. Replicator Selection and the Extended Phenotype 3. Zeitschrift für Tierpsychologie 47, 61–76 (1978).

  • 21.

    Gilbert, K. J., Nitta, J. H., Talavera, G. & Pierce, N. E. Keeping an eye on coloration: ecological correlates of the evolution of pitcher traits in the genus Nepenthes (Caryophyllales). Biological Journal of the Linnean Society 123, 321–327 (2018).

    • Article
    • Google Scholar
  • 22.

    McPherson, S., Robinson, A. & Fleischmann, A. Pitcher Plants of the Old World. 2, (Redfern Natural History Productions Dorset, 2009).

  • 23.

    Chin, L., Moran, J. A. & Clarke, C. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytologist 186, 461–470 (2010).

  • 24.

    Greenwood, M., Clarke, C., Lee, C. C., Gunsalam, A. & Clarke, R. H. A unique resource mutualism between the giant Bornean pitcher plant, Nepenthes rajah, and members of a small mammal community. PLoS ONE 6, e21114 (2011).

  • 25.

    Lim, Y. S. et al. How a pitcher plant facilitates roosting of mutualistic woolly bats. Evolutionary Ecology Research 16, 581–591 (2015).

    • Google Scholar
  • 26.

    Moran, J. A., Merbach, M. A., Livingston, N. J., Clarke, C. M. & Booth, W. E. Termite prey specialization in the pitcher plant Nepenthes albomarginata—evidence from stable isotope analysis. Annals of Botany 88, 307–311 (2001).

  • 27.

    Thorogood, C. J., Bauer, U. & Hiscock, S. J. Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytologist 217, 1035–1041 (2018).

  • 28.

    Adlassnig, W., Peroutka, M. & Lendl, T. Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann. Bot. 107, 181–94 (2011).

  • 29.

    Vacher, C. et al. The phyllosphere: microbial jungle at the plant-climate interface. Annual Review of Ecology, Evolution, and Systematics 47, 1–24 (2016).

    • Article
    • Google Scholar
  • 30.

    Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–40 (2012).

  • 31.

    Wagner, M. R. et al. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nature Communications 7, 12151 (2016).

  • 32.

    Renner, T. & Specht, C. D. Inside the trap: gland morphologies, digestive enzymes, and the evolution of plant carnivory in the Caryophyllales. Curr. Opin. Plant Biol. 16, 436–42 (2013).

  • 33.

    Ravee, R., Salleh, F. M. & Goh, H.-H. Discovery of digestive enzymes in carnivorous plants with focus on proteases. PeerJ 6, e4914 (2018).

  • 34.

    Buch, F., Kaman, W. E., Bikker, F. J., Yilamujiang, A. & Mithӧfer, A. Nepenthesin protease activity indicates digestive fluid dynamics in carnivorous Nepenthes plants. PloS One 10, e0118853 (2015).

  • 35.

    Athauda, S. B. P. et al. Enzymic and structural characterization of nepenthesin, a unique member of a novel subfamily of aspartic proteinases. Biochem. J. 381, 295–306 (2004).

  • 36.

    Buch, F. et al. Secreted pitfall-trap fluid of carnivorous Nepenthes plants is unsuitable for microbial growth. Annals of Botany 111, 375–383 (2012).

  • 37.

    Eilenberg, H. et al. Induced production of antifungal naphthoquinones in the pitchers of the carnivorous plant Nepenthes khasiana. J. Exp. Bot. 61, 911–22 (2010).

  • 38.

    Gaume, L. & Forterre, Y. A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS ONE 2, e1185 (2007).

  • 39.

    Moran, J. A., Gray, L. K., Clarke, C. & Chin, L. Capture mechanism in Palaeotropical pitcher plants (Nepenthaceae) is constrained by climate. Annals of Botany 112, 1279–1291 (2013).

  • 40.

    Bonhomme, V. et al. Slippery or sticky? Functional diversity in the trapping strategy of Nepenthes carnivorous plants. New Phytol. 191, 545–54 (2011).

  • 41.

    Bazile, V., Le Moguédec, G., Marshall, D. J. & Gaume, L. Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Annals of Botany 115, 705–716 (2015).

  • 42.

    McDonald, D., Pethick, D., Mullan, B. & Hampson, D. Increasing viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly-weaned pigs. British Journal of Nutrition 86, 487–498 (2001).

  • 43.

    Goddard, A. & Spiller, R. The effect of omeprazole on gastric juice viscosity, pH and bacterial counts. Alimentary Pharmacology & Therapeutics 10, 105–109 (1996).

  • 44.

    Umu, Ö. C. et al. Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations. Microbiome 3, 16 (2015).

  • 45.

    Amund, O. & Adebiyi, A. Effect of viscosity on the biodegradability of automotive lubricating oils. Tribology International 24, 235–237 (1991).

  • 46.

    Schneider, W. R. & Doetsch, R. N. Effect of viscosity on bacterial motility. J. Bacteriol. 117, 696–701 (1974).

  • 47.

    Moran, J. A., Hawkins, B. J., Gowen, B. E. & Robbins, S. L. Ion fluxes across the pitcher walls of three Bornean Nepenthes pitcher plant species: flux rates and gland distribution patterns reflect nitrogen sequestration strategies. Journal of Experimental Botany 61, 1365–1374 (2010).

  • 48.

    Rabotnova, I. L. The Importance of Physical-Chemical Factors (pH and rH2) for the Life Activity of Microorganisms. (1963).

  • 49.

    Rascovan, N. et al. Integrated analysis of root microbiomes of soybean and wheat from agricultural fields. Scientific Reports 6, 28084 (2016).

  • 50.

    Hartmann, A., Schmid, M., van Tuinen, D. & Berg, G. Plant-driven selection of microbes. Plant and Soil 321, 235–257 (2009).

  • 51.

    Dennis, P. G. et al. Linking rhizoplane pH and bacterial density at the microhabitat scale. J. Microbiol. Methods 76, 101–4 (2009).

  • 52.

    Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103, 626–631 (2006).

  • 53.

    Beasley, D. E., Koltz, A. M., Lambert, J. E., Fierer, N. & Dunn, R. R. The evolution of stomach acidity and its relevance to the human microbiome. PloS One 10, e0134116 (2015).

  • 54.

    Kanokratana, P. et al. Comparative Study of Bacterial Communities in Nepenthes. Microbial Ecology 72, 381–393 (2016).

  • 55.

    Bittleston, L. S. et al. Convergence between the microcosms of Southeast Asian and North American pitcher plants. Elife 7, e36741 (2018).

  • 56.

    Clarke, C. Nepenthes of Borneo. Kota Kinabalu, Sabah: Natural History Publications (Borneo) xi, 207p-col. illus. ISBN 1248185562 (1997).

  • 57.

    Bittleston, L. Commensals of Nepenthes pitchers. Carnivorous Plants: Physiology, Ecology, and Evolution. Oxford University Press. https://doi.org/10.1093/oso/9780198779841.003 23 (2018).

  • 58.

    Koopman, M. M., Fuselier, D. M., Hird, S. & Carstens, B. C. The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities. Appl. Environ. Microbiol. 76, 1851–60 (2010).

  • 59.

    Armitage, D. W. Linking the development and functioning of a carnivorous pitcher plant’s microbial digestive community. The ISME Journal 11, 2439 (2017).

  • 60.

    Miller, T. E. & terHorst, C. P. Testing successional hypotheses of stability, heterogeneity, and diversity in pitcher-plant inquiline communities. Oecologia 170, 243–51 (2012).

  • 61.

    Sambrook, J. & Russell, D. Molecular cloning: A Laboratory Manual, the third edition. (2001).

  • 62.

    Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6, 1621–4 (2012).

  • 63.

    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 108(Suppl 1), 4516–22 (2011).

  • 64.

    Amaral-Zettler, L. A., McCliment, E. A., Ducklow, H. W. & Huse, S. M. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE 4, e6372 (2009).

  • 65.

    Stoeck, T. et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19(Suppl 1), 21–31 (2010).

  • 66.

    Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–84 (1999).

  • 67.

    Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–45 (2003).

  • 68.

    Fritz, S. A. & Purvis, A. Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conservation Biology 24, 1042–1051 (2010).

  • 69.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. arXiv preprint arXiv 1406, 5823 (2014).

    • Google Scholar
  • 70.

    Oksanen, J. et al. Package “vegan.” Community ecology package, version 2 (2013).

  • 71.

    Mandal, S. et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microbial Ecology in Health and Disease 26, 27663 (2015).

  • 72.

    Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nature Biotechnology 36, 996–1004 (2018).

  • 73.

    Lee, H. et al. Reyranella terrae sp. nov., isolated from an agricultural soil, and emended description of the genus Reyranella. International Journal of Systematic and Evolutionary Microbiology 67, 2031–2035 (2017).

  • 74.

    Lloyd, F. E. The Carnivorous Plants. (Read Books Ltd, 2011).

  • 75.

    Saganová, M., Bokor, B., Stolárik, T. & Pavlovič, A. Regulation of enzyme activities in carnivorous pitcher plants of the genus Nepenthes. Planta 1–14 (2018).

  • 76.

    Bauer, U., Grafe, T. U. & Federle, W. Evidence for alternative trapping strategies in two forms of the pitcher plant, Nepenthes rafflesiana. J. Exp. Bot. 62, 3683–92 (2011).

  • 77.

    Collett, C. et al. A portable extensional rheometer for measuring the viscoelasticity of pitcher plant and other sticky liquids in the field. Plant Methods 11, 16 (2015).

  • 78.

    Baby, S., Johnson, A. J., Zachariah, E. J. & Hussain, A. A. Nepenthes pitchers are CO2-enriched cavities, emit CO2 to attract preys. Scientific Reports 7 (2017).

  • 79.

    Raj, G., Kurup, R., Hussain, A. A. & Baby, S. Distribution of naphthoquinones, plumbagin, droserone, and 5-O-methyl droserone in chitin-induced and uninduced Nepenthes khasiana: molecular events in prey capture. Journal of Experimental Botany 62, 5429–5436 (2011).

  • 80.

    Sanders, J. G. et al. Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Molecular Ecology 23, 1268–1283 (2014).

  • 81.

    Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

  • 82.

    Archetti, M. et al. Economic game theory for mutualism and cooperation. Ecol. Lett. 14, 1300–12 (2011).


  • Source: Ecology - nature.com

    Chance and necessity in the pleiotropic consequences of adaptation for budding yeast

    How plants protect themselves from sun damage