Gut shuttle service: endozoochory of dispersal-limited soil fauna by gastropods
- 609 Downloads
Numerous important ecosystem functions and services depend on soil biodiversity. However, little is known about the mechanisms which maintain the vast belowground biodiversity and about the filters shaping soil community composition. Yet, biotic interactions like facilitation and dispersal by animals are assumed to play a crucial role, particularly as most soil animal taxa are strongly limited in their active dispersal abilities. Here, we report on a newfound interaction of potentially high ubiquity and importance in soil communities: the endozoochorous dispersal of soil fauna by gastropods. We focus on the dispersal-limited group of oribatid mites, one of the most diverse and abundant soil animal groups. In a field survey in a German riparian forest, 73% of 40 collected slugs (Arion vulgaris) egested a total of 135 oribatid mites, belonging to 35 species. Notably, 70% of the egested mites were alive and survived the gut passage through slugs. Similar results were found for Roman snails (Helix pomatia), indicating the generality of our findings across different gastropod taxa. Complementary laboratory experiments confirmed our field observations, revealing that oribatid mites are, indeed, ingested and egested alive by slugs, and that they are able to independently escape the faeces and colonise new habitats. Our results strongly indicate that gastropods may help soil organisms to disperse within habitats, to overcome dispersal barriers, and to reach short-lived resource patches. Gastropods might even disperse whole multi-trophic micro-ecosystems, a discovery that could have profound implications for our understanding of dispersal mechanisms and the distribution of soil biodiversity.
KeywordsMicro-ecosystem dispersal Oribatid mites Seed dispersal Slugs Soil biodiversity
We are grateful to David Wardle and Wim van der Putten for their comments and suggestions on a previous version of the manuscript and Maria Feustel for her contribution to the surveys and experiments. Franz Horak and Bernhard Klarner identified oribatid and mesostigmatid mites, respectively. Julia Siebert identified protozoa, and Katja Steinauer the plants in the study area. Andrew Barnes improved the manuscript linguistically. MT and NE are supported by the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Research Foundation (DFG; FZT 118). ML is supported by the Max Planck Institute for Biogeochemistry, Jena, Germany and is funded by the German Research Foundation (DFG; FOR 456, FOR 1451–“The Jena Experiment”).
Author contribution statement
MT and NE conceived the study; MT performed the experiments and surveys; MT and ML analyzed the data; MT, ML, and NE wrote the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that there is no conflict of interest.
- Beck L, Horak F, Woas S (2014) Zur Taxonomie der Gattung Phthiracarus Perty, 1841 (Acari, Oribatida) in Südwestdeutschland. Carolinea 72:109–132Google Scholar
- Chmielewski W (1970) The passage of mites through the alimentary canal of vertebrates. Ekologia Polska 35:741–756Google Scholar
- Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9 and earlier. User’s Guide and application. http://purl.oclc.org/estimates
- Fox J, Weisberg S (2011) An R companion to applied regression. SAGE Publications, Thousand OaksGoogle Scholar
- Gulvik ME (2007) Mites (Acari) as indicators of soil biodiversity and land use monitoring: a review. Pol J Ecol 55:415–440Google Scholar
- Karg W (1993) Acari (Acarina), Milben. Parasitiformes (Anactinochaeta). Cohors Gamasina Leach. Raubmilben. In: Dahl F (ed) Die Tierwelt Deutschlands, 2nd edn. Gustav Fischer, JenaGoogle Scholar
- Kempson D, Lloyd M, Ghelardi R (1963) A new extractor for woodland litter. Pedobiologia 3:1–21Google Scholar
- Miko L, Stanko M (1991) Small mammals as carriers of non-parasitic mites (Oribatida, Uropodina). In: Dusbabek F, Bukva V (eds) Modern acarology: proceedings of the VIII International Congress of Acarology, České Buděkpvoce, Czechoslovakia, August 6–11, 1990. Academia, PragueGoogle Scholar
- Oksanen J, Blanchet FG, Friendly M et al (2016) vegan: community ecology package: ordination methods, diversity analysis and other functions for community and vegetation ecologists. https://cran.r-project.org/web/packages/vegan/index.html
- Petersen C, Hermann RJ, Barg MC et al (2015) Travelling at a slug’s pace: possible invertebrate vectors of Caenorhabditis nematodes. BMC Ecol 15. https://doi.org/10.1186/s12898-015-0050-z
- R Core Team (2016) R: a language and environment for statistical computing, vol 2016. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Schuppenhauer MM, Lehmitz R (2017) Floating islands: a method to detect aquatic dispersal and colonisation potential of soil microarthropods. Soil Org 89:119–126Google Scholar
- Thimm T, Hoffmann A, Borkott H, Munch JC, Tebbe CC (1998) The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Appl Environ Microb 64:2660–2669Google Scholar
- Totsching U, Schatz H (1997) Oribatid mites in a riverine forest near Glanz (Eastern Tyrol, Austria): Faunistics (Acari: Oribatida). Ber nat-med Verein Innsbruck 84:111–131Google Scholar
- Weigmann G (2006) Hornmilben (Oribatida). Goecke & Evers, KelternGoogle Scholar