Abstract
Environmental and ecological degradation can be monitored by biological indicators such as plants, yet little research has been done using subterranean organisms such as collembola, especially in cities. Collembola, a soil fauna group, can be used to assess soil quality and to decipher assembly rules of soil organisms in cities. Here, we review 75 articles on soil collembola in an urban context. We found that soil properties and landscape characteristics influenced soil communities. There is a need for more connectivity between green urban spaces to allow the dispersion of collembola. Little information is available on the assembly of collembola communities, on biotic interactions and on dynamics of colonisation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
André HM, Noti M-I, Lebrun P (1994) The soil fauna: the other last biotic frontier. Biodivers Conserv 3:45–56. https://doi.org/10.1007/BF00115332
Auclerc A, Ponge JF, Barot S, Dubs F (2009) Experimental assessment of habitat preference and dispersal ability of soil springtails. Soil Biol Biochem 41:1596–1604
Barot S, Abbadie L, Auclerc A, Barthélémy C, Bérille E, Billet P, Clergeau P, Consales J-N, Deschamp-Cottin M, David A, Devigne C, Dham V, Dusza Y, Gaillard A, Gonzalez E, Hédont M, Labarraque D, Le Bastard A-M, Morel J-L, Petit-Berghem Y, Rémy E, Rochelle-Newall E, Veyrières M (2019) Urban ecology, stakeholders and the future of ecology. Sci Total Environ 667:475–484. https://doi.org/10.1016/j.scitotenv.2019.02.410
Batty M (2008) The size, scale, and shape of cities. Science 319:769–771. https://doi.org/10.1126/science.1151419
Biffi S, De Souza CM, Firbank LG (2019) Epigeal fauna of urban food production sites show no obvious relationships with soil characteristics or site area. Agric Ecosyst Environ 286:106677. https://doi.org/10.1016/j.agee.2019.106677
Braaker S, Ghazoul J, Obrist MK, Moretti M (2014) Habitat connectivity shapes urban arthropod communities: the key role of green roofs. Ecology 95:1010–1021. https://doi.org/10.1890/13-0705.1
Brondizio ES, Settele J, Díaz S, Ngo HT (2019) Global assessment report on biodiversity and ecosystem services of the intergovernmental science-policy platform on biodiversity and ecosystem services. IPBES secretariat, Bonn, Germany (p 1148). https://doi.org/10.5281/zenodo.3831673
Burrow C, Pernin C, Lepretre A (2018) Influence of connectivity & topsoil management practices of a constructed technosol on pedofauna colonization: a field study. Appl Soil Ecol, HUMUSICA 3 - Rev Appl, Tools 123:416–419. https://doi.org/10.1016/j.apsoil.2017.12.001
Byrne LB (2007) Habitat structure: a fundamental concept and framework for urban soil ecology. Urban Ecosyst 10:255–274. https://doi.org/10.1007/s11252-007-0027-6
Byrne LB, Bruns MA (2004) The effects of lawn management on soil microarthropods. J Agric Urban Entomol 6:150–156
Cadotte MW, Yasui SL, Livingstone S, MacIvor JS (2017) Are urban systems beneficial, detrimental, or indifferent for biological invasion? Biol Invasion 19:3489–3503. https://doi.org/10.1007/s10530-017-1586-y
Christiansen K, Doyle M, Kahlert M, Gobaleza D, (1992) Interspecific interactions between collembolan populations in culture. Pedobiologia.
Clobert J, Baguette M, Benton TG, Bullock JM (eds) (2012) Dispersal ecology and evolution. Oxford University Press, Oxford, New York
Culik MP, Filho DZ (2003) Diversity and distribution of Collembola (Arthropoda: Hexapoda) of Brazil. Biodivers Conserv 12:1119–1143. https://doi.org/10.1023/A:1023069912619
de Groot RS, Wilson MA, Boumans RMJ (2002) A typology for the classification, description and valuation of ecosystem functions, goods and services. Ecol Econ 41:393–408. https://doi.org/10.1016/S0921-8009(02)00089-7
Decaëns T, Jiménez JJ, Gioia C, Measey GJ, Lavelle P (2006) The values of soil animals for conservation biology. Eur J Soil Biol 42:S23–S38. https://doi.org/10.1016/j.ejsobi.2006.07.001
Delamare Deboutteville C (1947) Note faunistique sur les Collemboles de France. Revue française d’Entomologie 2:125–138
Drake JA (1990) Communities as assembled structures: Do rules govern pattern? Trends Ecol Evol 5:159–164. https://doi.org/10.1016/0169-5347(90)90223-Z
Dunger W (1998) Immigration, Ansiedlung und Primärsukzession der Bodenfauna auf jungen Kippböden. In: Pflug W (ed) Braunkohlentagebau und Rekultivierung: Landschaftsökologie — Folgenutzung — Naturschutz. Springer, Berlin, Heidelberg
Dunger W, Schulz, H-J, Zimdars B, (2002) Colonization behaviour of Collembola under different conditions of dispersal: Proceedings of the Xth international Colloquium on Apterygota, České Budějovice 2000: Apterygota at the Beginning of the Third Millennium. Pedobiologia 46: 316–327. doi: https://doi.org/10.1078/0031-4056-00139
Dupont L, Torres-Leguizamon M, René-Corail P, Mathieu J (2017) Landscape features impact connectivity between soil populations: a comparative study of gene flow in earthworms. Mol Ecol 26:3128–3140. https://doi.org/10.1111/mec.14102
Eitminaviciute I (2006) Microarthropod communities in anthropogenic urban soils 2 Seasonal dynamics of microarthropod number in crossing curb soils. Zoologichesky Zhurnal 3:1309–1320
Fountain MT, Hopkin SP (2004) A Comparative study of the effects of metal contamination on collembola in the field and in the laboratory. Ecotoxicology 13:573–587. https://doi.org/10.1023/B:ECTX.0000037194.66321.2c
Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trend Ecol Evol 15:369–372. https://doi.org/10.1016/S0169-5347(00)01940-6
Ge B, Mehring AS, Levin LA (2019) Urbanization alters belowground invertebrate community structure in semi-arid regions: a comparison of lawns, biofilters and sage scrub. Landsc Urban Plan 192:103664. https://doi.org/10.1016/j.landurbplan.2019.103664
Giller PS (1996) The diversity of soil communities, the ‘poor man’s tropical rainforest.’ Biodivers Conserv 5:135–168. https://doi.org/10.1007/BF00055827
Grubert D, Butenschoen O, Maraun M, Scheu S (2016) Understanding earthworm – Collembola interactions and their importance for ecosystem processes needs consideration of species identity. Eur J Soil Biol 77:60–67. https://doi.org/10.1007/s00374-004-0782-y
Guilland C, Maron PA, Damas O, Ranjard L (2018) Biodiversity of urban soils for sustainable cities. Environ Chem Lett. https://doi.org/10.1007/s10311-018-0751-6
Hopkin SP (1997) Biology of the Springtails: (Insecta: Collembola). Oxford University Press, Oxford
Huang C, Wang T, Luo Y, Chen S, Kim KC (2013) Assessing collembola biodiversity under human influence at three Gorges Area, China. Environ Entomol 42:214–222. https://doi.org/10.1603/EN12253
Islam MS, Hossain M, Hossain M, Yasmin M (2018) Impact of climatic factors and soil quality on the abundance and population density of Collembola in the Rajshahi University Campus, Bangladesh. J Entomol Zool Stud 6:1119–1125
Janion-Scheepers C, Deharveng L, Bedos A, Chown SL (2015) Updated list of Collembola species currently recorded from South Africa. ZooKeys. https://doi.org/10.3897/zookeys.503.8966
Jaskuła R, Sulikowska-Drozd A, Jabłońska A, Banaś K, Rewicz T (2019) Undesirable immigrants: hobbyist vivaria as a potential source of alien invertebrate species. PeerJ 7:e7617. https://doi.org/10.7717/peerj.7617
Jensen P, Jacobson GL, Willard DE (1973) Effects of mowing and raking on Collembola. Ecology 54:564–572. https://doi.org/10.2307/1935341
Joimel S, Cortet J, Jolivet CC, Saby NPA, Chenot ED, Branchu P, Consalès JN, Lefort C, Morel JL, Schwartz C (2016) Physico-chemical characteristics of topsoil for contrasted forest, agricultural, urban and industrial land uses in France. Sci Total Environ 545:40–47. https://doi.org/10.1016/j.scitotenv.2015.12.035
Joimel S, Schwartz C, Hedde M, Kiyota S, Krogh PH, Nahmani J, Pérès G, Vergnes A, Cortet J (2017) Urban and industrial land uses have a higher soil biological quality than expected from physicochemical quality. Sci Total Environ 584:614–621. https://doi.org/10.1016/j.scitotenv.2017.01.086
Joimel S, Grard B, Auclerc A, Hedde M, Le Doaré N, Salmon S, Chenu C (2018) Are Collembola “flying” onto green roofs? Ecol Eng 111:117–124
Joimel S, Schwartz C, Maurel N, Magnus B, Machon N, Bel J, Cortet J (2019) Contrasting homogenization patterns of plant and collembolan communities in urban vegetable gardens. Urban Ecosyst. https://doi.org/10.1007/s11252-019-00843-z
Lang A (2000) The pitfalls of pitfalls: a comparison of pitfall trap catches and absolute density estimates of epigeal invertebrate predators in Arable Land. J Pest Sci 73:99–106. https://doi.org/10.1007/BF02956438
Liu Z, He C, Zhou Y, Wu J (2014) How much of the world’s land has been urbanized, really? a hierarchical framework for avoiding confusion. Landscape Ecol 29:763–771. https://doi.org/10.1007/s10980-014-0034-y
Lortie CJ, Brooker RW, Choler P, Kikvidze Z, Michalet R, Pugnaire FI, Callaway RM (2004) Rethinking plant community theory. Oikos 107:433–438. https://doi.org/10.1111/j.0030-1299.2004.13250.x
Maisto G, Milano V, Santorufo L (2017) Relationships among site characteristics, taxonomical structure and functional trait distribution of arthropods in forest, urban and agricultural soils of Southern Italy. Ecol Res 32:511–521. https://doi.org/10.1007/s11284-017-1464-1
Marzluff JM (2019) A decadal review of urban ornithology and a prospectus for the future. Ibis. https://doi.org/10.1111/ibi.12430@10.1111/(ISSN)1474-919X.highly_cited_us_research
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176. https://doi.org/10.1007/s11252-007-0045-4
MEA, Reid WV, Mooney HA, Cropper A, Capistrano D, Carpenter SR, Chopra K, Dasgupta P, Dietz T, Duraiappah AK, Hassan R, Kasperson R, Leemans R, Ma R, Mcmichael A, Pingali P, Samper, C, Scholes R, Watson R, Zakri AH, Zurek MB (2005) Millenium ecosystem assessment synthesis report. Washington D.C, Island Press
Milano V, Cortet J, Baldantoni D, Bellino A, Dubs F, Nahmani J, Strumia S, Maisto G (2017) Collembolan biodiversity in Mediterranean urban parks: impact of history, urbanization, management and soil characteristics. Appl Soil Ecol 119:428–437. https://doi.org/10.1016/j.apsoil.2017.03.022
Milano V, Maisto G, Baldantoni D, Bellino A, Bernard C, Croce A, Dubs F, Strumia S, Cortet J (2018) The effect of urban park landscapes on soil Collembola diversity: a Mediterranean case study. Landsc Urban Plan 180:135–147. https://doi.org/10.1016/j.landurbplan.2018.08.008
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Annal Entomol Soc Am 93:825–835
Mo W, Li Y, Guo J, Zhang R (2018) Faunal communities of deep soil layers in suburban, Beijing. Biodivers Sci 26:248–257
Morel JL, Chenu C, Lorenz K (2014) Ecosystem services provided by soils of urban, industrial, traffic, mining, and military areas (SUITMAs). J Soils Sediments. https://doi.org/10.1007/s11368-014-0926-0
Natuhara Y, Imai C, Takeda H (1994) Classification and ordination of communities of soil arthropods in an urban park of Osaka City. Ecol Res 9:131–141. https://doi.org/10.1007/BF02347488
Nielsen UN, Osler GHR, Campbell CD, Burslem DFRP, van der Wal R (2010) The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. J Biogeogr 37:1317–1328. https://doi.org/10.1111/j.1365-2699.2010.02281.x
Pomorski RJ, Skarzynski DS, (1996) (Collembola) pól uprawnych, ziemi doniczrjwej, szklarni i pieczarkarni – klucz do oznaczania // Diagnostyka czkodników roslin i ich wrogów naturalnych.
Ponge J-F (2013) Disturbances, organisms and ecosystems: a global change perspective. Ecol Evol 3:1113–1124. https://doi.org/10.1002/ece3.505
Ponge J-F, Gillet S, Dubs F, Fedoroff E, Haese L, Sousa JP, Lavelle P (2003) Collembolan communities as bioindicators of land use intensification. Soil Biol Biochem 35:813–826. https://doi.org/10.1016/S0038-0717(03)00108-1
Ponge J-F, Dubs F, Gillet S, Sousa JP, Lavelle P (2006) Decreased biodiversity in soil springtail communities: the importance of dispersal and landuse history in heterogeneous landscapes. Soil Biol Biochem 38:1158–1161. https://doi.org/10.1016/j.soilbio.2005.09.004
Qin Z, Xie JF, Quan GM, Zhang JE, Mao DJ, Wang JX (2019) Changes in the soil meso- and micro-fauna community under the impacts of exotic Ambrosia artemisiifolia. Ecol Res 34:265–276. https://doi.org/10.1111/1440-1703.1271
Querner P, Bruckner A (2010) Combining pitfall traps and soil samples to collect Collembola for site scale biodiversity assessments. Appl Soil Ecol 45:293–297. https://doi.org/10.1016/j.apsoil.2010.05.005
Querner P, Milasowszky N, Zulka KP, Abensperg-Traun M, Willner W, Sauberer N, Jakomini C, Wrbka T, Schmitzberger I, Zechmeister HG (2018) Habitat structure, quality and landscape predict species richness and communities of collembola in dry grasslands in Austria. Insects 9:81. https://doi.org/10.3390/insects9030081
Ramalho CE, Hobbs RJ (2012) Time for a change: dynamic urban ecology. Trends Ecol Evol 27:179–188. https://doi.org/10.1016/j.tree.2011.10.008
Rantalainen M-L, Haimi J, Fritze H, Pennanen T, Setälä H (2008) Soil decomposer community as a model system in studying the effects of habitat fragmentation and habitat corridors. Soil Biol Biochem 40:853–863. https://doi.org/10.1016/j.soilbio.2007.11.008
Rochefort S, Shetlar DJ, Brodeur J (2013) Impact of four turf management regimes on arthropod abundance in lawns. Pest Manag Sci 69:54–65. https://doi.org/10.1002/ps.3361
Rota E, Caruso T, Migliorini M, Monaci F, Agamennone V, Biagini G, Bargagli R (2015) Diversity and abundance of soil arthropods in urban and suburban holm oak stands. Urban Ecosyst 18:715–728. https://doi.org/10.1007/s11252-014-0425-5
Rowles AD, O’Dowd DJ (2009) Impacts of the invasive Argentine ant on native ants and other invertebrates in coastal scrub in south-eastern Australia. Austral Ecol 34:239–248. https://doi.org/10.1111/j.1442-9993.2008.01922.x
Rumble H, Gange AC (2013) Soil microarthropod community dynamics in extensive green roofs. Ecol Eng 57:197–204. https://doi.org/10.1016/j.ecoleng.2013.04.012
Rumble H, Finch P, Gange AC (2018) Green roof soil organisms: anthropogenic assemblages or natural communities? Appl Soil Ecol 126:11–20. https://doi.org/10.1016/j.apsoil.2018.01.010
Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219. https://doi.org/10.1023/A:1008887817883
Rzeszowski K (2017) The effects of anthropogenic disturbances and hydrological activity of a river on soil Collembola communities in an urbanized zone. Eur J Soil Biol 82:116–120. https://doi.org/10.1016/j.ejsobi.2017.09.004
Rzeszowski K, Sterzyńska M (2016) Changes through time in soil Collembola communities exposed to urbanization. Urban Ecosyst 19:143–158. https://doi.org/10.1007/s11252-015-0478-0
Rzeszowski K, Zadrożny P, Nicia P (2017) The effect of soil nutrient gradients on Collembola communities inhabiting typical urban green spaces. Pedobiologia 64:15–24. https://doi.org/10.1016/j.pedobi.2017.06.003
Salmon S (2004) The impact of earthworms on the abundance of Collembola: improvement of food resources or of habitat? Biol Fertil Soils 40:323–333. https://doi.org/10.1007/s00374-004-0782-y
Salmon S, Rebuffat S, Prado S, Sablier M, D’Haese C, Sun J-S, Ponge J-F (2019) Chemical communication in springtails: a review of facts and perspectives. Biol Fertil Soils 55:425–438. https://doi.org/10.1007/s00374-019-01365-8
Santorufo L, Van Gestel CAM, Rocco A, Maisto G (2012) Soil invertebrates as bioindicators of urban soil quality. Environ Pollut 161:57–63. https://doi.org/10.1016/j.envpol.2011.09.042
Santorufo L, Cortet J, Arena C, Goudon R, Rakoto A, Morel J-L, Maisto G (2014a) An assessment of the influence of the urban environment on collembolan communities in soils using taxonomy- and trait-based approaches. Appl Soil Ecol 78:48–56. https://doi.org/10.1016/j.apsoil.2014.02.008
Santorufo L, Van Gestel CAM, Maisto G (2014b) Sampling season affects conclusions on soil arthropod community structure responses to metal pollution in Mediterranean urban soils. Geoderma 226–227:47–53. https://doi.org/10.1016/j.geoderma.2014.02.001
Santorufo L, Cortet J, Nahmani J, Pernin C, Salmon S, Pernot A, Morel JL, Maisto G (2015) Responses of functional and taxonomic collembolan community structure to site management in Mediterranean urban and surrounding areas. Eur J Soil Biol 70:46–57. https://doi.org/10.1016/j.ejsobi.2015.07.003
Santorufo L, Joimel S, Auclerc A, Deremiens J, Grisard G, Hedde M, Nahmani J, Pernin C, Cortet J (2021) Early colonization of constructed technosol by microarthropods. Ecol Eng 162:106174. https://doi.org/10.1016/j.ecoleng.2021.106174
Schindler BY, Vasl A, Blaustein L, Gurevich D, Kadas GJ, Seifan M (2019) Fine-scale substrate heterogeneity does not affect arthropod communities on green roofs. PeerJ 7:e6445. https://doi.org/10.7717/peerj.6445
Schrader S, Böning M (2006) Soil formation on green roofs and its contribution to urban biodiversity with emphasis on Collembolans. Pedobiologia 50:347–356. https://doi.org/10.1016/j.pedobi.2006.06.003
Shochat E, Warren PS, Faeth SH, Mcintyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191
Shrubovych J (2002) The fauna of springtails (Collembola) in Lviv. Vestnik Zoologii 36:63–67
Sousa JP, da Gama MM, Pinto C, Keating A, Calhôa F, Lemos M, Castro C, Luz T, Leitão P, Dias S (2004) Effects of land-use on Collembola diversity patterns in a Mediterranean landscape. Pedobiologia 48:609–622. https://doi.org/10.1016/j.pedobi.2004.06.004
Sterzynska M (1987) Structure of springtail (Collembola) communities in the urban green of Warsaw. Memorabilia Zoologica 6:3–18
Sterzynska M (1990) Communities of Collembola in natural and transformed soils of the linden- oak-hornbeam sites of the mazovian lowland Poland. Fragmenta Faunistica (warsaw) 34:165–262
Sterzyńska M, Nicia P, Zadrożny P, Fiera C, Shrubovych J, Ulrich W (2018) Urban springtail species richness decreases with increasing air pollution. Ecol Ind 94:328–335. https://doi.org/10.1016/j.ecolind.2018.06.063
Sukopp H (2008) On the Early History of Urban Ecology in Europe. In: Marzluff JM, Shulenberger E, Endlicher W, Alberti M, Bradley G, Ryan C, Simon U, ZumBrunnen C (eds) Urban ecology: an international perspective on the interaction between humans and nature. Springer, Boston
Theenhaus A, Scheu S, Schaefer M (1999) Contramensal interactions between two collembolan species: effects on population development and on soil processes. Funct Ecol 13:238–246. https://doi.org/10.1046/j.1365-2435.1999.00303.x
Thibaud J-M, D’Haese C (2010) Le petit Collembole illustré. Bulletin de l’Association Entomologique d’Auvergne 1–56
Tresch S, Frey D, Le Bayon R-C, Zanetta A, Rasche F, Fliessbach A, Moretti M (2019) Litter decomposition driven by soil fauna, plant diversity and soil management in urban gardens. Sci Total Environ 658:1614–1629. https://doi.org/10.1016/j.scitotenv.2018.12.235
Vincent Q, Leyval C, Beguiristain T, Auclerc A (2018) Functional structure and composition of Collembola and soil macrofauna communities depend on abiotic parameters in derelict soils. Appl Soil Ecol 130:259–270. https://doi.org/10.1016/j.apsoil.2018.07.002
Vucic-Pestic O, Birkhofer K, Rall BC, Scheu S, Brose U (2010) Habitat structure and prey aggregation determine the functional response in a soil predator–prey interaction. Pedobiologia 53:307–312. https://doi.org/10.1016/j.pedobi.2010.02.003
Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886. https://doi.org/10.1111/j.1461-0248.2006.00931.x
Wickenbrock L, Heisler C (1997) Influence of earthworm activity on the abundance of collembola in soil. Soil Biol Biochem 29:517–521. https://doi.org/10.1016/S0038-0717(96)00175-7
Yi Z, Jinchao F, Dayuan X, Weiguo S, Axmacher JC (2012) A comparison of terrestrial arthropod sampling methods. Jore 3:174–182. https://doi.org/10.5814/j.issn.1674-764x.2012.02.010
Young RF, Wolf SA (2006) Goal attainment in urban ecology research: a bibliometric review 1975–2004. Urban Ecosyst 9:179–193. https://doi.org/10.1007/s11252-006-8589-2
Zobel M (1997) The relative of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends Ecol Evol 12:266–269. https://doi.org/10.1016/S0169-5347(97)01096-3
Funding
This work was supported by the lab recherche environnement VINCI ParisTech.
Author information
Authors and Affiliations
Contributions
SJ: idea for the article. AJ, SJ: literature search and data analysis. AJ, SJ: drafted the manuscript. LVG: critically revised the work.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Joimel, S., Jules, A. & Vieublé Gonod, L. Collembola dispersion, selection, and biological interactions in urban ecosystems: a review. Environ Chem Lett 20, 2123–2133 (2022). https://doi.org/10.1007/s10311-022-01406-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10311-022-01406-z