Shells of the Roman snail are important microhabitats for soil invertebrates
DOI:
https://doi.org/10.25674/so93iss3id167Keywords:
Gastropoda, Helix pomatia, shell adopter, shelter, soil animalsAbstract
Shells of molluscs from snail farms (heliciculture) are used as food additives or construction material and ecological engineering approaches utilize their potential to assist with ecosystem restoration. Previous studies, for example, highlighted the importance of snail shells as microhabitat for threatened arthropod species with particular focus on wild bees nesting in empty shells. This study focuses on shells of the Roman snail (Helix pomatia Linnaeus, 1758) and their value as microhabitat for shell adopters in different dominant vegetation forms and sample periods. In total, 1408 empty shells were placed in areas dominated by one of two vegetation forms (herbaceous vegetation or trees) from February to November 2019 (autumn) or from February to June/July 2020 (summer). All collected shells (N = 618) were sealed at the time of collection, frozen and all content was then analysed with a digital microscope. In total, 91.4 % of all collected shells were occupied and the average number of shell adopters was 1.5 time higher in shells collected in summer compared to shells collected in autumn. The number of shell adopters per shell was 1.5 times higher in study areas dominated by herbaceous vegetation compared to study areas dominated by trees. Shell width, but not shell height significantly affected the composition of shell adopter communities. Shells with a larger width were more frequently colonized by another gastropod species [Discus rotundatus (O. F. Müller, 1774)] than less wide shells. Shells of the Roman snail provide important multipurpose benefits for a wide range of soil organisms, particularly in habitats that were dominated by herbaceous vegetation and in summer. In autumn, shell adopters included isopods, gastropods and spiders in one subset of shells or Collembola in another subset. The future use of commercially available, empty shells from heliciculture in local restoration projects of open, tree-free areas, holds the potential to support a diverse invertebrate fauna with additional refuge habitats.
References
Anderson, M. J. (2017): Permutational multivariate analysis of variance (PERMANOVA). – Wiley statsref: statistics reference online: 1–15 [http://doi.org/10.1002/9781118445112.stat07841].
Bogusch, P., J. Roháček, P. Baňař, A. Astapenková, O. Kouklík, P. Pech, P. Janšta, K. Heller, L. Hlaváčková & P. Heneberg (2019): The presence of high numbers of empty shells in anthropogenic habitats is insufficient to attract shell adopters among the insects. – Insect Conservation and Diversity 12: 193–205 [http://doi.org/10.1111/icad.12335].
Bogusch, P., L. Hlaváčková, N. R. Gasol & P. Heneberg (2020): Near-natural habitats near almond orchards with presence of empty gastropod shells are important for solitary shell-nesting bees and wasps. – Agriculture, Ecosystems and Environment 299: 106949 [http://doi.org/10.1016/j.agee.2020.106949].
Bogusch, P., L. Hlaváčková, K. Šilhán & M. Horsák (2020): Long‑term changes of steppe‑associated wild bees differ between shell‑nesting and ground‑nesting species. – Journal of Insect Conservation 24: 513–523 [http://doi.org/10.1007/s10841-020-00232-4].
Broly, P., J. - L. Deneubourg & C. Devigne (2013): Benefits of aggregation in woodlice: a factor in the terrestrialization process? – In Insectes Sociaux 60: 419–435 [http://doi.org/10.1007/s00040-013-0313-7].
Dias, N., M. Hassall, & T. Waite (2012): The influence of microclimate on foraging and sheltering behaviours of terrestrial isopods: Implications for soil carbon dynamics under climate change. – Pedobiologia 55: 137–144 [http://doi.org/10.1016/j.pedobi.2011.10.003].
Dromph, K. M. (2001): Dispersal of enthomopathogenic fungi by collembolans. – Soil Biology & Biochemistry 33: 2047-2051 [http://doi.org/10.1016/s0038-0717(01)00130-4].
Forte, A., A. Zucaro, G. De Vico & A. Fierro (2016): Carbon footprint of heliciculture: A case study from an Italian experimental farm. – Agricultural Systems 142: 99–111 [http://doi.org/10.1016/j.agsy.2015.11.010].
Gess, F. W. & S. K. Gess (1999): The use by wasps, bees and spiders of shells of Trigonephrus Pilsb. (Mollusca: Gasteropoda: Dorcasiidae) in desertic winter-rainfall areas in southern Africa. – Journal of Arid Environments 43: 143–153 [http://doi.org/10.1006/jare.1999.0549].
Gutiérrez, J. L., C. G. Jones, D. L. Strayer & O. O. Iribarne (2003): Molluscs as ecosystem engineers: the role of shell production in aquatic habitats. – Oikos 101(1): 79–90 [DOI 10.1034/j.1600-0706.2003.12322.x].
Hanlon, R. D. G. (1981): Influence of grazing by Collembola on the activity of senescent fungal colonies grown on media of different nutrient concentration. – Oikos 36 (3): 362-367 [http://doi.org/10.1007/s00442-006-0538-5].
Hansen, R. A. (1999): Red oak litter promotes a microarthropod functional group that accelerates its decomposition. – Plant and Soil 209: 37–45 [http://doi.org/10.1023/A:1004506414711].
Hassall, A. & J. M. Tuck (2007): Sheltering behavior of terrestrial isopods in grasslands. – Invertebrate Biology 126(1): 46–56 [http://doi.org/10.1111/j.1744-7410.2007.00075.x].
Hassall, M., A. Moss, B. Dixie & J. J. Gilroy (2018): Interspecific variation in responses to microclimate by terrestrial isopods: implications in relation to climate change. – ZooKeys 801: 5–24 [http://doi.org/10.3897/zookeys.801.24934].
Heneberg, P., P. Bogusch & L. Hlavačkova (2020): Experimental confirmation of empty snail shells as limiting resources for specialized bees and wasps. – Ecological Engineering 142: 105640 [http://doi.org/10.1016/j.ecoleng.2019.105640].
Hopfenmüller, S., A. Holzschuh & I. Steffan-Dewenter (2020): Effects of grazing intensity, habitat area and connectivity on snail-shell nesting bees. – Biological Conservation 242: 108406 [http://doi.org/10.1016/j.biocon.2020.108406].
Keppel, G., S. Anderson, C. Williams, S. Kleindorfer & C. O’Connell (2017): Microhabitats and canopy cover moderate high summer temperatures in a fragmented Mediterranean landscape. – PLoS ONE 12(8): e0183106 [http://doi.org/10.1371/journal.pone.0183106].
Kolenda, K., S. Salata, K. Kujawa, N. Kuśmierek, A. Smolis & M. Kadej (2020): Deadly trap or sweet home? The case of discarded containers as novelty microhabitats for ants. – Global Ecology and Conservation 23: e01064 [http://doi.org/10.1016/j.gecco.2020.e01064].
Leclercq-Dransarta, J., C. Pernina, S. Demuyncka, F. Grumiauxa, S. Lemièrea & A. Leprêtrea (2019): Isopod physiological and behavioral responses to drier conditions: An experiment with four species in the context of global warming. – European Journal of Soil Biology 90: 22–30 [http://doi.org/10.1016/j.ejsobi.2018.11.005].
Moreno-Rueda, G. (2007): Refuge selection by two sympatric species of arid-dwelling land snails: Different adaptive strategies to achieve the same objective. – Journal of Arid Environments 68: 588–598 [http://doi.org/10.1016/j.jaridenv.2006.08.004].
Moreno-Rueda, G., C. Marfil-Daza, F. J. Ortiz-Sanchez & A. Melic (2008): Weather and the use of empty gastropod shells by arthropods. – Annales de la Société entomologique de France (N.S.) 44 (3): 373–377 [http://doi.org/10.1080/00379271.2008.10697573].
Müller, A., Praz, C. & A. Dorchin (2018): Biology of Palaearctic Wainia bees of the subgenus Caposmia including a short review on snail shell nesting in osmiine bees (Hymenoptera, Megachilidae). – Journal of Hymenoptera Research 65:
–89 [http://doi.org/10.3897/jhr.65.27704].
Norton, B. A., L. J. Thomson, N. S. G. Williams & M. J. McDonnell (2014): The effect of urban ground covers on arthropods: An experiment. – Urban Ecosystem 17: 77–99 [http://doi.org/10.1007/s11252-013-0297-0].
Perry, R. W. (2013): Potential energy expenditure by litter-roosting bats associated with temperature under leaf litter during winter. – Journal of Thermal Biology 38: 467–473 [http://doi.org/10.1016/j.jtherbio.2013.08.007].
Potts, S.G., B. Vulliamy, S. Roberts, C. O’Toole, A. Dafni, G. Ne’Eman & P. Willmer (2005): Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. – Ecological Entomology 30: 78–85 [http://doi.org/10.1111/j.0307-6946.2005.00662.x].
Romero, D., C. Ornosa & P. Vargas (2020): Where and why? Bees, snail shells and climate: Distribution of Rhodanthidium (Hymenoptera: Megachilidae) in the Iberian Peninsula. – Entomological Science 23: 256–270 [http://doi.org/10.1111/ens.12420].
Rupp, U. & A. Ziegler (2019): The effect of exuviae ingestion on lysosomal calcium accumulation and the presence of exosomes in the hepatopancreas of Porcellio scaber. – Journal of Structural Biology 208: 107392 [http://doi.org/10.1016/j.jsb.2019.09.009].
Søvik, G. & H. P. Leinaas (2003): Long life cycle and high adult survival in an arctic population of the mite Ameronothrus lineatus (Acari, Oribatida) from Svalbard. – Polar Biology 26: 500–508 [http://doi.org/10.1007/s00300-003-0510-3].
Søvik, G., H. P. Leinaas, R. A. Ims & T. Solhøy (2003): Population dynamics and life history of the oribatid mite Ameronothrus lineatus (Acari, Oribatida) on the high arctic archipelago of Svalbard. – Pedobiologia 47: 257–271 [http://doi.org/10.1078/0031-4056-00189].
Spohn, M., Golte-Bechtle, M. & Spohn, R. (2008) Was blüht denn da?. – Kosmos Verlag: 492 pp.
Tluste, C., U. Bröring, T. Němec & K. Birkhofer (2020): Morphometric traits of shells determine external attack and internal utilization marks in the Roman snail in eastern Germany. – Web Ecology 20: 1–8 [http://doi.org/10.5194/we-20-1-2020].
Wollmann, E. (2002): Botanische Studien zu den Sachsendorfer Wiesen. – Cottbus. – In: R. Striegler, W.-D. Heym & B. Schneider (eds). – Natur und Landschaft in der Niederlausitz 22: 95–116.
Downloads
Published
How to Cite
Issue
Section
License
All articles from Senckenberg’s SOIL ORGANISMS Open Access scientific journal that are made available on the Senckenberg website (www.senckenberg.de) and also www.soil-organisms.org may be read, copied, distributed, and (in limited quantity) printed for non-commercial, private, scientific purposes.
In accordance with the German Science Foundation’s „Rules for the Safeguarding of Good Scientific Practice“, references to cited articles are to be complete and correct and furnished with a link to the website of the Senckenberg journal in question.
The Senckenberg Society for Nature Research (Senckenberg Gesellschaft für Naturforschung, SGN) is a member of the Leibniz Association (Leibniz-Gemeinschaft) and is therefore committed to the idea of Open Access as explained in the Berlin Declaration (Berlin Declaration on Open Access to Scientific Knowledge, Berliner Erklärung über den offenen Zugang zu wissenschaftlichem Wissen).
Open Access is understood to mean the charge-exempt public access to scientific results via the internet. The users should be able to read, copy, print, search within, and reference the full text without limitation and to use it in any conceivable lawful manner without financial, legal or technical hindrance.
This applies also to the SGN, which publishes various scientific series. Some scientific journals are made available to the public via Open Acess in addition to printed copies.
