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      Travelling at a slug’s pace: possible invertebrate vectors of Caenorhabditis nematodes

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          Abstract

          Background

          How do very small animals with limited long-distance dispersal abilities move between locations, especially if they prefer ephemeral micro-habitats that are only available for short periods of time? The free-living model nematode Caenorhabditis elegans and several congeneric taxa appear to be common in such short-lived environments, for example decomposing fruits or other rotting plant material. Dispersal is usually assumed to depend on animal vectors, yet all current data is based on only a limited number of studies. In our project we performed three comprehensive field surveys on possible invertebrate vectors in North German locations containing populations of C. elegans and two related species, especially C. remanei, and combined these screens with an experimental analysis of persistence in one of the vector taxa.

          Results

          Our field survey revealed that Caenorhabditis nematodes are commonly found in slugs, isopods, and chilopods, but are not present in the remaining taxonomic groups examined. Surprisingly, the nematodes were frequently isolated from the intestines of slugs, even if slugs were not collected in close association with suitable substrates for Caenorhabditis proliferation. This suggests that the nematodes are able to enter the slug intestines and persist for certain periods of time. Our experimental analysis confirmed the ability of C. elegans to invade slug intestines and subsequently be excreted alive with the slug feces, although only for short time periods under laboratory conditions.

          Conclusions

          We conclude that three invertebrate taxonomic groups represent potential vectors of Caenorhabditis nematodes. The nematodes appear to have evolved specific adaptations to enter and persist in the harsh environment of slug intestines, possibly indicating first steps towards a parasitic life-style.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12898-015-0050-z) contains supplementary material, which is available to authorized users.

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          Most cited references37

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            The natural history of Caenorhabditis elegans.

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              Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae

              Background The nematode Caenorhabditis elegans is a major model organism in laboratory biology. Very little is known, however, about its ecology, including where it proliferates. In the past, C. elegans was mainly isolated from human-made compost heaps, where it was overwhelmingly found in the non-feeding dauer diapause stage. Results C. elegans and C. briggsae were found in large, proliferating populations in rotting plant material (fruits and stems) in several locations in mainland France. Both species were found to co-occur in samples isolated from a given plant species. Population counts spanned a range from one to more than 10,000 Caenorhabditis individuals on a single fruit or stem. Some populations with an intermediate census size (10 to 1,000) contained no dauer larvae at all, whereas larger populations always included some larvae in the pre-dauer or dauer stages. We report on associated micro-organisms, including pathogens. We systematically sampled a spatio-temporally structured set of rotting apples in an apple orchard in Orsay over four years. C. elegans and C. briggsae were abundantly found every year, but their temporal distributions did not coincide. C. briggsae was found alone in summer, whereas both species co-occurred in early fall and C. elegans was found alone in late fall. Competition experiments in the laboratory at different temperatures show that C. briggsae out-competes C. elegans at high temperatures, whereas C. elegans out-competes C. briggsae at lower temperatures. Conclusions C. elegans and C. briggsae proliferate in the same rotting vegetal substrates. In contrast to previous surveys of populations in compost heaps, we found fully proliferating populations with no dauer larvae. The temporal sharing of the habitat by the two species coincides with their temperature preference in the laboratory, with C. briggsae populations growing faster than C. elegans at higher temperatures, and vice at lower temperatures.
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                Author and article information

                Contributors
                cpetersen@zoologie.uni-kiel.de
                ruben.hrmnn@hotmail.com
                m.barg85@gmx.de
                rebecca.schalkowski@googlemail.com
                pdirksen@zoologie.uni-kiel.de
                cbarbosa@zoologie.uni-kiel.de
                hschulenburg@zoologie.uni-kiel.de
                Journal
                BMC Ecol
                BMC Ecol
                BMC Ecology
                BioMed Central (London )
                1472-6785
                13 July 2015
                13 July 2015
                2015
                : 15
                : 19
                Affiliations
                Department of Evolutionary Ecology and Genetics, Zoological Institute Christian-Albrechts University, Am Botanischen Garten 1-9, 24118 Kiel, Germany
                Article
                50
                10.1186/s12898-015-0050-z
                4501285
                26170141
                48eecd5b-d5c2-4f76-b597-38e769ab997b
                © Petersen et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 21 February 2015
                : 18 June 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Ecology
                caenorhabditis elegans,caenorhabditis remanei,phoresy,commensalism,parasitism,arion,vector-mediated migration,ephemeral habitats

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