Advertisement

Oecologia

, Volume 186, Issue 3, pp 655–664 | Cite as

Gut shuttle service: endozoochory of dispersal-limited soil fauna by gastropods

  • Manfred Türke
  • Markus Lange
  • Nico Eisenhauer
Behavioral ecology –original research

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.

Keywords

Micro-ecosystem dispersal Oribatid mites Seed dispersal Slugs Soil biodiversity 

Notes

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”).

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.

Supplementary material

442_2018_4058_MOESM1_ESM.pdf (4.5 mb)
Supplementary material 1 (PDF 4584 kb)
442_2018_4058_MOESM2_ESM.xlsx (36 kb)
Supplementary material 2 (XLSX 36 kb)

References

  1. Anderson JM (1978) Inter-habitat and intra-habitat relationships between woodland Cryptostigmata species-diversity and diversity of soil and litter microhabitats. Oecologia 32:341–348CrossRefPubMedGoogle Scholar
  2. Astrom J, Bengtsson J (2011) Patch size matters more than dispersal distance in a mainland-island metacommunity. Oecologia 167:747–757CrossRefPubMedGoogle Scholar
  3. Astrom J, Part T (2013) Negative and matrix-dependent effects of dispersal corridors in an experimental metacommunity. Ecology 94:72–82CrossRefPubMedGoogle Scholar
  4. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511CrossRefPubMedGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  6. Beck L, Horak F, Woas S (2014) Zur Taxonomie der Gattung Phthiracarus Perty, 1841 (Acari, Oribatida) in Südwestdeutschland. Carolinea 72:109–132Google Scholar
  7. Boch S, Prati D, Werth S, Rüetschi J, Fischer M (2011) Lichen endozoochory by snails. PLos One 6:e18770CrossRefPubMedPubMedCentralGoogle Scholar
  8. Boch S, Berlinger M, Fischer M et al (2013) Fern and bryophyte endozoochory by slugs. Oecologia 172:817–822CrossRefPubMedGoogle Scholar
  9. Boch S, Fischer M, Knop E, Allan E (2014) Endozoochory by slugs can increase bryophyte establishment and species richness. Oikos 124:331–336CrossRefGoogle Scholar
  10. Butin H (1981) Der „Schwarze Rindenschorf” der Buche, verursacht durch Ascodichaena rugosa Butin. Eur J For Pathol 11:299–305CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. Chmielewski W (1970) The passage of mites through the alimentary canal of vertebrates. Ekologia Polska 35:741–756Google Scholar
  13. 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
  14. 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 5:3–21CrossRefGoogle Scholar
  15. 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 110:14296–14301CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183CrossRefGoogle Scholar
  17. Figuerola J, Green AJ, Santamaria L (2003) Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Glob Ecol Biogeogr 12:427–436CrossRefGoogle Scholar
  18. Fox J, Weisberg S (2011) An R companion to applied regression. SAGE Publications, Thousand OaksGoogle Scholar
  19. Gan H, Zak DR, Hunter MD (2014) Trophic stability of soil oribatid mites in the face of environmental change. Soil Biol Biochem 68:71–77CrossRefGoogle Scholar
  20. Gish M, Ben-Ari M, Inbar M (2017) Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence, significance, and prospectus. Oecologia 183:347–352CrossRefPubMedGoogle Scholar
  21. Green AJ, Sanchez MI (2006) Passive internal dispersal of insect larvae by migratory birds. Biol Lett 2:55–57CrossRefPubMedGoogle Scholar
  22. Gulvik ME (2007) Mites (Acari) as indicators of soil biodiversity and land use monitoring: a review. Pol J Ecol 55:415–440Google Scholar
  23. Hämäläinen A, Broadley K, Droghini A et al (2017) The ecological significance of secondary seed dispersal by carnivores. Ecosphere 8:e01685CrossRefGoogle Scholar
  24. 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 14:117–122CrossRefGoogle Scholar
  25. 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
  26. Kempson D, Lloyd M, Ghelardi R (1963) A new extractor for woodland litter. Pedobiologia 3:1–21Google Scholar
  27. 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 106:339–350CrossRefGoogle Scholar
  28. 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 Google Scholar
  29. Kokko H, Lopez-Sepulcre A (2006) From individual dispersal to species ranges: perspectives for a changing world. Science 313:789–791CrossRefPubMedGoogle Scholar
  30. Lebedeva N, Krivolutsky D (2003) Birds spread soil microarthropods to Arctic islands. Dokl Biol Sci 391:329–332CrossRefPubMedGoogle Scholar
  31. Lehmitz R, Russell D, Hohberg K, Christian A, Xylander WER (2011) Wind dispersal of oribatid mites as a mode of migration. Pedobiologia 54:201–207CrossRefGoogle Scholar
  32. Lehmitz R, Russell D, Hohberg K, Christian A, Xylander WER (2012) Active dispersal of oribatid mites into young soils. Appl Soil Ecol 55:10–19CrossRefGoogle Scholar
  33. Lindo Z, Winchester NN (2009) Spatial and environmental factors contributing to patterns in arboreal and terrestrial oribatid mite diversity across spatial scales. Oecologia 160:817–825CrossRefPubMedGoogle Scholar
  34. Lopez LCS, Gonçalves DA, Mantovani A, Rios RI (2002) Bromeliad ostracods pass through amphibian (Scinaxax perpusillus) and mammalian guts alive. Hydrobiologia 485:209–211CrossRefGoogle Scholar
  35. Mack TN, Andraso G (2015) Ostracods and other prey survive passage through the gut of round goby (Neogobius melanostomus). J Great Lakes Res 41:303–306CrossRefGoogle Scholar
  36. Maraun M, Erdmann G, Fischer BM et al (2011) Stable isotopes revisited: their use and limits for oribatid mite trophic ecology. Soil Biol Biochem 43:877–882CrossRefGoogle Scholar
  37. 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
  38. 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 279:1061–1067CrossRefGoogle Scholar
  39. Moore PD (1999) Ecology—a shrike for mobility. Nature 397:21–23CrossRefGoogle Scholar
  40. Norton RA (1980) Observations on phoresy by oribatid mites (Acari: Oribatei). Int J Acarol 6:121–130CrossRefGoogle Scholar
  41. Ojala R, Huhta V (2001) Dispersal of microarthropods in forest soil. Pedobiologia 45:443–450CrossRefGoogle Scholar
  42. 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
  43. Otsuki H, Yano S (2014) Potential lethal and non-lethal effects of predators on dispersal of spider mites. Exp Appl Acarol 64:265–275CrossRefPubMedGoogle Scholar
  44. 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
  45. R Core Team (2016) R: a language and environment for statistical computing, vol 2016. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. 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 50:518–528CrossRefPubMedGoogle Scholar
  47. 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 36:1769–1774CrossRefGoogle Scholar
  48. 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
  49. 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 82:422–426CrossRefGoogle Scholar
  50. Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552CrossRefPubMedGoogle Scholar
  51. 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 Google Scholar
  52. 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
  53. 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
  54. Turchetti T, Chelazzi G (1984) Possible role of slugs as vectors of the chestnut blight fungus. Eur J For Pathol 14:125–127CrossRefGoogle Scholar
  55. Türke M, Heinze E, Andreas K, Svendsen SM, Gossner MM, Weisser WW (2010) Seed consumption and dispersal of ant-dispersed plants by slugs. Oecologia 163:681–693CrossRefPubMedGoogle Scholar
  56. Türke M, Andreas K, Gossner MM et al (2012) Are gastropods, rather than ants, important dispersers of seeds of myrmecochorous forest herbs? Am Nat 179:124–131CrossRefPubMedGoogle Scholar
  57. 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:e32292CrossRefPubMedPubMedCentralGoogle Scholar
  58. Veresoglou SD, Halley JM, Rillig MC (2015) Extinction risk of soil biota. Nat Commun 6:8862CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wada S, Kawakami K, Chiba S (2012) Snails can survive passage through a bird’s digestive system. J Biogeogr 39:69–73CrossRefGoogle Scholar
  60. 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 111:5266–5270CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wall DH, Nielsen UN, Six J (2015) Soil biodiversity and human health. Nature 528:69–76PubMedGoogle Scholar
  62. Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886CrossRefPubMedGoogle Scholar
  63. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633CrossRefPubMedGoogle Scholar
  64. Weigmann G (2006) Hornmilben (Oribatida). Goecke & Evers, KelternGoogle Scholar
  65. 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 83:101–108CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  2. 2.Institute of BiologyLeipzig UniversityLeipzigGermany
  3. 3.Max Planck Institute for BiogeochemistryJenaGermany

Personalised recommendations