Abstract
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.
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References
Anderson JM (1978) Inter-habitat and intra-habitat relationships between woodland Cryptostigmata species-diversity and diversity of soil and litter microhabitats. Oecologia 32:341–348
Astrom J, Bengtsson J (2011) Patch size matters more than dispersal distance in a mainland-island metacommunity. Oecologia 167:747–757
Astrom J, Part T (2013) Negative and matrix-dependent effects of dispersal corridors in an experimental metacommunity. Ecology 94:72–82
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beck L, Horak F, Woas S (2014) Zur Taxonomie der Gattung Phthiracarus Perty, 1841 (Acari, Oribatida) in Südwestdeutschland. Carolinea 72:109–132
Boch S, Prati D, Werth S, Rüetschi J, Fischer M (2011) Lichen endozoochory by snails. PLos One 6:e18770
Boch S, Berlinger M, Fischer M et al (2013) Fern and bryophyte endozoochory by slugs. Oecologia 172:817–822
Boch S, Fischer M, Knop E, Allan E (2014) Endozoochory by slugs can increase bryophyte establishment and species richness. Oikos 124:331–336
Butin H (1981) Der „Schwarze Rindenschorf” der Buche, verursacht durch Ascodichaena rugosa Butin. Eur J For Pathol 11:299–305
Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2(2):art24. https://doi.org/10.1890/es10-00117.1
Chmielewski W (1970) The passage of mites through the alimentary canal of vertebrates. Ekologia Polska 35:741–756
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
Colwell RK, Chao A, Gotelli NJ et al (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21
de Vries FT, Thebault E, Liiri M et al (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci USA 110:14296–14301
Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183
Figuerola J, Green AJ, Santamaria L (2003) Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Glob Ecol Biogeogr 12:427–436
Fox J, Weisberg S (2011) An R companion to applied regression. SAGE Publications, Thousand Oaks
Gan H, Zak DR, Hunter MD (2014) Trophic stability of soil oribatid mites in the face of environmental change. Soil Biol Biochem 68:71–77
Gish M, Ben-Ari M, Inbar M (2017) Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence, significance, and prospectus. Oecologia 183:347–352
Green AJ, Sanchez MI (2006) Passive internal dispersal of insect larvae by migratory birds. Biol Lett 2:55–57
Gulvik ME (2007) Mites (Acari) as indicators of soil biodiversity and land use monitoring: a review. Pol J Ecol 55:415–440
Hämäläinen A, Broadley K, Droghini A et al (2017) The ecological significance of secondary seed dispersal by carnivores. Ecosphere 8:e01685
Karasawa S, Gotoh K, Sasaki T, Hijii N (2005) Wind-based dispersal of oribatid mites (Acari: Oribatida) in a subtropical forest in Japan. J Acarol Soc Japan 14:117–122
Karg W (1993) Acari (Acarina), Milben. Parasitiformes (Anactinochaeta). Cohors Gamasina Leach. Raubmilben. In: Dahl F (ed) Die Tierwelt Deutschlands, 2nd edn. Gustav Fischer, Jena
Kempson D, Lloyd M, Ghelardi R (1963) A new extractor for woodland litter. Pedobiologia 3:1–21
Knee W, Forbes MR, Beaulieu F (2013) Diversity and host use of mites (Acari: Mesostigmata, Oribatida) phoretic on bark beetles (Coleoptera: Scolytinae): global generalists, local specialists? Ann Entomol Soc Am 106:339–350
Knop E, Rindlisbacher N, Ryser S, Gruebler MU (2013) Locomotor activity of two sympatric slugs: implications for the invasion success of terrestrial invertebrates. Ecosphere. https://doi.org/10.1890/es13-00154.1
Kokko H, Lopez-Sepulcre A (2006) From individual dispersal to species ranges: perspectives for a changing world. Science 313:789–791
Lebedeva N, Krivolutsky D (2003) Birds spread soil microarthropods to Arctic islands. Dokl Biol Sci 391:329–332
Lehmitz R, Russell D, Hohberg K, Christian A, Xylander WER (2011) Wind dispersal of oribatid mites as a mode of migration. Pedobiologia 54:201–207
Lehmitz R, Russell D, Hohberg K, Christian A, Xylander WER (2012) Active dispersal of oribatid mites into young soils. Appl Soil Ecol 55:10–19
Lindo Z, Winchester NN (2009) Spatial and environmental factors contributing to patterns in arboreal and terrestrial oribatid mite diversity across spatial scales. Oecologia 160:817–825
Lopez LCS, Gonçalves DA, Mantovani A, Rios RI (2002) Bromeliad ostracods pass through amphibian (Scinaxax perpusillus) and mammalian guts alive. Hydrobiologia 485:209–211
Mack TN, Andraso G (2015) Ostracods and other prey survive passage through the gut of round goby (Neogobius melanostomus). J Great Lakes Res 41:303–306
Maraun M, Erdmann G, Fischer BM et al (2011) Stable isotopes revisited: their use and limits for oribatid mite trophic ecology. Soil Biol Biochem 43:877–882
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, Prague
Miura O, Torchin ME, Bermingham E, Jacobs DK, Hechinger RF (2012) Flying shells: historical dispersal of marine snails across Central America. Proc Roy Soc B Biol Sci 279:1061–1067
Moore PD (1999) Ecology—a shrike for mobility. Nature 397:21–23
Norton RA (1980) Observations on phoresy by oribatid mites (Acari: Oribatei). Int J Acarol 6:121–130
Ojala R, Huhta V (2001) Dispersal of microarthropods in forest soil. Pedobiologia 45:443–450
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
Otsuki H, Yano S (2014) Potential lethal and non-lethal effects of predators on dispersal of spider mites. Exp Appl Acarol 64:265–275
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, Vienna
Renker C, Otto P, Schneider K, Zimdars B, Maraun M, Buscot F (2005) Oribatid mites as potential vectors for soil microfungi: study of mite-associated fungal species. Microb Ecol 50:518–528
Schneider K, Migge S, Norton RA et al (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (N-15/N-14). Soil Biol Biochem 36:1769–1774
Schuppenhauer MM, Lehmitz R (2017) Floating islands: a method to detect aquatic dispersal and colonisation potential of soil microarthropods. Soil Org 89:119–126
Simonova J, Simon OP, Kapic S, Nehasil L, Horsak M (2016) Medium-sized forest snails survive passage through birds’ digestive tract and adhere strongly to birds’ legs: more evidence for passive dispersal mechanisms. J Moll Stud 82:422–426
Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552
Tesson SV, Okamura B, Dudaniec RY et al (2016) Integrating microorganism and macroorganism dispersal: modes, techniques and challenges with particular focus on co-dispersal. Écoscience. https://doi.org/10.1080/11956860.2016.1148458
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 64:2660–2669
Totsching U, Schatz H (1997) Oribatid mites in a riverine forest near Glanz (Eastern Tyrol, Austria): Faunistics (Acari: Oribatida). Ber nat-med Verein Innsbruck 84:111–131
Turchetti T, Chelazzi G (1984) Possible role of slugs as vectors of the chestnut blight fungus. Eur J For Pathol 14:125–127
Türke M, Heinze E, Andreas K, Svendsen SM, Gossner MM, Weisser WW (2010) Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia 163:681–693
Türke M, Andreas K, Gossner MM et al (2012) Are gastropods, rather than ants, important dispersers of seeds of myrmecochorous forest herbs? Am Nat 179:124–131
van Leeuwen CHA, van der Velde G, van Lith B, Klaassen M (2012) Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds. PLoS One 7:e32292
Veresoglou SD, Halley JM, Rillig MC (2015) Extinction risk of soil biota. Nat Commun 6:8862
Wada S, Kawakami K, Chiba S (2012) Snails can survive passage through a bird’s digestive system. J Biogeogr 39:69–73
Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111:5266–5270
Wall DH, Nielsen UN, Six J (2015) Soil biodiversity and human health. Nature 528:69–76
Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886
Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633
Weigmann G (2006) Hornmilben (Oribatida). Goecke & Evers, Keltern
Zaitsev AS, Gongalsky KB, Persson T, Bengtsson J (2014) Connectivity of litter islands remaining after a fire and unburnt forest determines the recovery of soil fauna. Appl Soil Ecol 83:101–108
Acknowledgements
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”).
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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.
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Communicated by Liliane Ruess.
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Türke, M., Lange, M. & Eisenhauer, N. Gut shuttle service: endozoochory of dispersal-limited soil fauna by gastropods. Oecologia 186, 655–664 (2018). https://doi.org/10.1007/s00442-018-4058-x
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DOI: https://doi.org/10.1007/s00442-018-4058-x