Impacts of climate change – simulated flooding and drought events – on terrestrial invertebrates (Enchytraeids and Collembolans)

Rita C. Bicho, Janeck J. Scott-Fordsmand, Mónica J.B. Amorim

PDF(1343 KB)
PDF(1343 KB)
Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (1) : 240262. DOI: 10.1007/s42832-024-0262-2
RESEARCH ARTICLE

Impacts of climate change – simulated flooding and drought events – on terrestrial invertebrates (Enchytraeids and Collembolans)

Author information +
History +

Highlights

● Impacts of soil moisture levels from 10% to 100% on two soil invertebrates.

E. crypticus and F. candida survived at extreme scenarios (10% and 100%).

● For both species, reproduction was severely reduced in extreme scenarios.

● Higher adaptative phenotypic plasticity for F. candida compared to E. crypticus .

Abstract

Knowledge on impacts of climate change on soil invertebrate communities is scarce. Amongst the biggest challenges are the increase in temperature and arid regions, while at the same time, in other parts of the planet, extreme precipitation events and flooding occur. The aim of the present study was to investigate the impacts of drought and flooding in soil invertebrates. Enchytraeus crypticus and Folsomia candida, model ecotoxicology test-species (OECD) were used to assess performance (survival, reproduction, size) in LUFA 2.2 soil moistened to 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90%, 100% of the soil water holding capacity (WHC). Overall, both species had high tolerance for drought and flooding scenarios, with survival threshold for E. crypticus being between 10% and 90% moisture and for F. candida being between 10% and 100% moisture. Reproduction decreased from moisture ≤30% and >70% moisture. In drought there was a decrease on adults’ size, for both species from ≤30% moisture. The morphological adaptations observed support evidence of adaptative phenotypic plasticity for both species, but highest for F. candida. A redistribution of soil invertebrate species can be expected to occur, this under the present and future climate change scenarios, with new and more tolerant species to prevail in different habitats. This will impact not only soil biodiversity structure, but also its function.

Graphical abstract

Keywords

climate change / soil moisture / phenotypic plasticity / biodiversity / ecosystem services

Cite this article

Download citation ▾
Rita C. Bicho, Janeck J. Scott-Fordsmand, Mónica J.B. Amorim. Impacts of climate change – simulated flooding and drought events – on terrestrial invertebrates (Enchytraeids and Collembolans). Soil Ecology Letters, 2025, 7(1): 240262 https://doi.org/10.1007/s42832-024-0262-2

References

[1]
Abrahamsen, G., 1971. The influence of temperature and soil moisture on the population density of Cognettia sphagnetorum [Oligochaeta: Enchytraeidae] in cultures with homogenized raw humus. Pedobiologia11, 417–424.
CrossRef Google scholar
[2]
Albaladejo, J., Díaz-Pereira, E., de Vente, J., 2021. Eco-holistic soil conservation to support land degradation neutrality and the sustainable development goals. CATENA196, 104823.
CrossRef Google scholar
[3]
Amorim, M.J.B., Gansemans, Y., Gomes, S.I.L., Van Nieuwerburgh, F., Scott-Fordsmand, J.J., 2021. Annelid genomes: Enchytraeus crypticus, a soil model for the innate (and primed) immune system. Lab Animal50, 285–294.
CrossRef Google scholar
[4]
Amundson, R., Berhe, A.A., Hopmans, J.W., Olson, C., Sztein, A.E., Sparks, D.L., 2015. Soil and human security in the 21st century. Science348, 6235.
CrossRef Google scholar
[5]
Bandow, C., Karau, N., Römbke, J., 2014. Interactive effects of pyrimethanil, soil moisture and temperature on Folsomia candida and Sinella curviseta (Collembola). Applied Soil Ecology81, 22–29.
CrossRef Google scholar
[6]
Barrett, J.E., Virginia, R.A., Wall, D.H., Adams, B.J., 2008. Decline in a dominant invertebrate species contributes to altered carbon cycling in a low-diversity soil ecosystem. Global Change Biology14, 1734–1744.
CrossRef Google scholar
[7]
Bicho, R.C., Faustino, A.M.R., Rêma, A., Scott-Fordsmand, J.J., Amorim, M.J.B., 2021. Confirmatory assays for transient changes of omics in soil invertebrates – Copper materials in a multigenerational exposure. Journal of Hazardous Materials402, 123500.
CrossRef Google scholar
[8]
Bicho, R.C., Roelofs, D. Mariën, J., Scott-Fordsmand, J.J., Amorim, M.J.B., 2020a. Epigenetic effects of (nano)materials in environmental species – Cu case study in Enchytraeus crypticus. Environment International136, 105447.
CrossRef Google scholar
[9]
Bicho, R.C., Scott-Fordsmand, J.J., Amorim, M.J.B., 2020b. Developing an epigenetics model species - From blastula to mature adult, life cycle methylation profile of Enchytraeus crypticus (Oligochaete). Science of the Total Environment732, 139079.
CrossRef Google scholar
[10]
Briones, M.J.I., Ineson, P., Piearce, T.G., 1997. Effects of climate change on soil fauna; responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Applied Soil Ecology6, 117–134.
CrossRef Google scholar
[11]
Ciobanu, M., Eisenhauer, N., Stoica, I.A., Cesarz, S., 2019. Natura 2000 priority and non-priority habitats do not differ in soil nematode diversity. Applied Soil Ecology135, 166–173.
CrossRef Google scholar
[12]
Coyle, D.R., Nagendra, U.J., Taylor, M.K., Campbell, J.H., Cunard, C.E., Joslin, A.H., Mundepi, A., Phillips, C.A., Callaham ., M.A.Jr., 2017. Soil fauna responses to natural disturbances, invasive species, and global climate change: current state of the science and a call to action. Soil Biology and Biochemistry110, 116–133.
CrossRef Google scholar
[13]
Cragg, R.G., Bardgett, R.D., 2001. How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biology and Biochemistry33, 2073–2081.
CrossRef Google scholar
[14]
da Silva, P.M., Nascimento, E., Reis, F., Briones, M.J.I., Brussaard, L., Sousa, J.P., 2020. More frequent droughts slow down litter decomposition across European agroecosystems and increase the importance of earthworm functional diversity. Applied Soil Ecology153, 103628.
CrossRef Google scholar
[15]
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C., Martin, P.R., 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America105, 6668–6672.
CrossRef Google scholar
[16]
Dözsa-Farkas, K., 1977. Beobachtungen über die Trockenheitstoleranz von Fridericia galba (Oligochaeta, Enchytraeidae). Opusc Zool Budapest 14, 77–83.
[17]
Duncan, E.J., Leask, M.P., Dearden, P.K., 2020. Genome architecture facilitates phenotypic plasticity in the honeybee (Apis mellifera). Molecular Biology and Evolution37, 1964–1978.
CrossRef Google scholar
[18]
Eekhout, J.P.C., de Vente, J., 2022. Global impact of climate change on soil erosion and potential for adaptation through soil conservation. Earth-Science Reviews226, 103921.
CrossRef Google scholar
[19]
European Commission, 2019. World Atlas of Desertification [Online]. (accessed May 24, 2019).
[20]
Faddeeva-Vakhrusheva, A., Kraaijeveld, K., Derks, M.F.L., Anvar, S.Y., Agamennone, V., Suring, W., Kampfraath, A.A., Ellers, J., Le Ngoc, G., van Gestel, C.A.M., Mariën, Smit, S., van Straalen, N.M., Roelofs, D., 2017. Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genomics18, 493.
CrossRef Google scholar
[21]
Fountain, M.T., Hopkin, S.P., 2005. Folsomia candida (collembola): a “standard” soil arthropod. Annual Review of Entomology50, 201–222.
CrossRef Google scholar
[22]
Fusco, G., Minelli, A., 2010. Phenotypic plasticity in development and evolution: facts and concepts. Philosophical Transactions of the Royal Society B: Biological Sciences365, 547–556.
CrossRef Google scholar
[23]
Guarino, F., Cicatelli, A., Castiglione, S., Agius, D.R., Orhun, G.E., Fragkostefanakis, S., Leclercq, J., Dobránszki, J., Kaiserli, E., Lieberman-Lazarovich, M., Sõmera, M., Sarmiento, C., Vettori, C., Paffetti, D., Poma, A.M.G., Moschou, P.N., Gašparović, M., Yousefi, S., Vergata, C., Berger, M.M.J., Gallusci, P., Miladinović, D., Martinelli, F., 2022. An epigenetic alphabet of crop adaptation to climate change. Frontiers in Genetics13, 818727.
CrossRef Google scholar
[24]
Guerra, C.A., Bardgett, R.D., Caon, L., Crowther, T.W., Delgado-Baquerizo, M., Montanarella, L., Navarro, L.M., Orgiazzi, A., Singh, B.K., Tedersoo, L., Vargas-Rojas, R., Briones, M.J.I., Buscot, F., Cameron, E.K., Cesarz, S., Chatzinotas, A., Cowan, D.A., Djukic, I., van den Hoogen, J., Lehmann, A., Maestre, F.T., Marín, C., Reitz, T., Rillig, M.C., Smith, L.C., de Vries, F.T., Weigelt, A., Wall, D.H., Eisenhauer, N., 2021. Tracking, targeting, and conserving soil biodiversity. Science371, 239–241.
CrossRef Google scholar
[25]
Holmstrup, M., Bayley, M., 2013. Protaphorura tricampata, a euedaphic and highly permeable springtail that can sustain activity by osmoregulation during extreme drought. Journal of Insect Physiology59, 1104–1110.
CrossRef Google scholar
[26]
Holmstrup, M., Sjursen, H., Ravn, H., Bayley, M., 2001. Dehydration tolerance and water vapour absorption in two species of soil-dwelling Collembola by accumulation of sugars and polyols. Functional Ecology15, 647–653.
CrossRef Google scholar
[27]
Holmstrup, M., Slotsbo, S., Rozsypal, J., Henriksen, P.G., Bayley, M., 2015. Accumulation of free amino acids during exposure to drought in three springtail species. Journal of Insect Physiology82, 114–121.
CrossRef Google scholar
[28]
Holmstrup, M., Sørensen, J.G., Dai, W.C., Krogh, P.H., Schmelz, R.M., Slotsbo, S., 2022. Analysis of heat and cold tolerance of a freeze-tolerant soil invertebrate distributed from temperate to Arctic regions: evidence of selection for extreme cold tolerance. Journal of Comparative Physiology B192, 435–445.
CrossRef Google scholar
[29]
Huey, R.B., Deutsch, C.A., Tewksbury, J.J., Vitt, L.J., Hertz, P.E., Álvarez Pérez, H.J., Garland, T., 2009. Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences276, 1939–1948.
CrossRef Google scholar
[30]
Kærsgaard, C.W., Holmstrup, M., Malte, H., Bayley, M., 2004. The importance of cuticular permeability, osmolyte production and body size for the desiccation resistance of nine species of Collembola. Journal of Insect Physiology50, 5–15.
CrossRef Google scholar
[31]
Kaka, H., Opute, P.A., Maboeta, M.S., 2021. Potential impacts of climate change on the toxicity of pesticides towards earthworms. Journal of Toxicology2021, 8527991.
CrossRef Google scholar
[32]
Korobushkin, D.I., Guseva, P.A., Gongalsky, K.B., Saifutdinov, R.A., Zaitsev, A.S., Degtyarev, M.I., 2024. Are there different trophic niches of enchytraeids? A stable isotopic (δ13C, δ15N) evidence. Soil Biology and Biochemistry194, 109422.
CrossRef Google scholar
[33]
Lagerlöf, J., Strandh, M., 1997. Hatching of Enchytraeidae (Oligochaeta) from egg cocoons in agricultural soil exposed to different drought regimes - a laboratory study. Pedobiologia41, 334–341.
CrossRef Google scholar
[34]
Lalejini, A., Ferguson, A.J., Grant, N.A., Ofria, C., 2021. Adaptive phenotypic plasticity stabilizes evolution in fluctuating environments. Frontiers in Ecology and Evolution9, 715381.
CrossRef Google scholar
[35]
Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Blouin, M., Bureau, F., Margerie, P., Mora, P., Rossi, J.P., 2006. Soil invertebrates and ecosystem services. European Journal of Soil Biology42, S3–S15.
CrossRef Google scholar
[36]
Leal Filho, W., Nagy, G.J., Setti, A.F.F., Sharifi, A., Donkor, F.K., Batista, K., Djekic, I., 2023. Handling the impacts of climate change on soil biodiversity. Science of the Total Environment869, 161671.
CrossRef Google scholar
[37]
Lussenhop, J., 1996. Collembola as mediators of microbial symbiont effects upon soybean. Soil Biology and Biochemistry28, 363–369.
CrossRef Google scholar
[38]
Ma, Y.Y., Liu, H., Yu, Y., Guo, L., Zhao, W.Z., Yetemen, O., 2022. Revisiting soil water potential: towards a better understanding of soil and plant interactions. Water14, 3721.
CrossRef Google scholar
[39]
Maraldo, K., Holmstrup, M., 2009. Recovery of enchytraeid populations after severe drought events. Applied Soil Ecology42, 227–235.
CrossRef Google scholar
[40]
Maraldo, K., Holmstrup, M., 2010. Enchytraeids in a changing climate: a mini-review. Pedobiologia53, 161–167.
CrossRef Google scholar
[41]
Maraldo, K., Ravn, H.W., Slotsbo, S., Holmstrup, M., 2009. Responses to acute and chronic desiccation stress in Enchytraeus (Oligochaeta: Enchytraeidae). Journal of Comparative Physiology B179, 113–123.
CrossRef Google scholar
[42]
Maraldo, K., Schmidt, I.K., Beier, C., Holmstrup, M., 2008. Can field populations of the enchytraeid, Cognettia sphagnetorum, adapt to increased drought stress? Soil Biology and Biochemistry 40, 1765–1771.
[43]
Marx, M.T., Guhmann, P., Decker, P., 2012. Adaptations and predispositions of different middle european arthropod taxa (collembola, araneae, chilopoda, diplopoda) to flooding and drought conditions. Animals2, 564–590.
CrossRef Google scholar
[44]
Marx, M.T., Wild, A.K., Knollmann, U., Kamp, G., Wegener, G., Eisenbeis, G., 2009. Responses and adaptations of collembolan communities (Hexapoda: Collembola) to flooding and hypoxic conditions. Pesquisa Agropecuária Brasileira44, 1002–1010.
[45]
Miner, B.G., Sultan, S.E., Morgan, S.G., Padilla, D.K., Relyea, R.A., 2005. Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution20, 685–692.
CrossRef Google scholar
[46]
OECD, 2016a. Test No. 220: Enchytraeid Reproduction Test. OECD (OECD Guidelines for the Testing of Chemicals, Section 2). DOI:10.1787/9789264264472-en.
[47]
OECD, 2016b. Test No. 232: Collembolan Reproduction Test in Soil. OECD (OECD Guidelines for the Testing of Chemicals, Section 2). DOI:10.1787/9789264264601-en.
[48]
Paul, R.J., Colmorgen, M., Hüller, S., Tyroller, F., Zinkler, D., 1997. Circulation and respiratory control in millimetre-sized animals (Daphnia magna, Folsomia candida) studied by optical methods. Journal of Comparative Physiology B167, 399–408.
CrossRef Google scholar
[49]
Pelosi, C., Römbke, J., 2018. Enchytraeids as bioindicators of land use and management. Applied Soil Ecology123, 775–779.
CrossRef Google scholar
[50]
Pereira, H.M., Navarro, L.M., Martins, I.S., 2012. Global biodiversity change: the bad, the good, and the unknown. Annual Review of Environment and Resources37, 25–50.
CrossRef Google scholar
[51]
Peterson, J.W., Johnson, E.M., Cencer, J.L., Thomason, C.J., 2006. Physiochemical conditions of Folsomia candida occurrence in a shallow coastal Lake Michigan aquifer. Environmental Geology49, 1125–1138.
CrossRef Google scholar
[52]
Pigliucci, M., 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution 20, 481–486.
[53]
Pimentel, D., 2006. Soil erosion: a food and environmental threat. Environment, Development and Sustainability8, 119–137.
CrossRef Google scholar
[54]
Plum, N.M., Filser, J., 2005. Floods and drought: response of earthworms and potworms (Oligochaeta: Lumbricidae, Enchytraeidae) to hydrological extremes in wet grassland. Pedobiologia49, 443–453.
CrossRef Google scholar
[55]
Potapov, A., Bellini, B., Chown, S., Deharveng, L., Janssens, F., Kováč, L., Kuznetsova, N., Ponge, J.F., Potapov, M., Querner, P., Russell, D., Sun, X., Zhang, F., Berg, M., 2020. Towards a global synthesis of Collembola knowledge- challenges and potential solutions. Soil Organisms92, 161–188.
CrossRef Google scholar
[56]
Schilthuizen, M., Kellermann, V., 2014. Contemporary climate change and terrestrial invertebrates: evolutionary versus plastic changes. Evolutionary Applications7, 56–67.
CrossRef Google scholar
[57]
Schlichting, C.D., Wund, M.A., 2014. Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evolution68, 656–672.
CrossRef Google scholar
[58]
Schmidt, A., John, K., Arida, G., Auge, H., Brandl, R., Horgan, F.G., Hotes, S., Marquez, L., Radermacher, N., Settele, J., Wolters, V., Schädler, M., 2015. Effects of residue management on decomposition in irrigated rice fields are not related to changes in the decomposer community. PLoS One10, e0134402.
CrossRef Google scholar
[59]
Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods9, 671–675.
CrossRef Google scholar
[60]
SigmaPlot, 1997. Statistical Package for the Social Sciences e SigmaPlot for Windows. Chicago: IL, USA .
[61]
Silva, A.R.R., Malheiro, C., Loureiro, S., González-Alcaraz, M.N., 2022. Toxicity of historically metal(loid)-contaminated soils to Folsomia candida under the influence of climate change alterations. Environmental Pollution305, 119256.
CrossRef Google scholar
[62]
Singh, J., Schädler, M., Demetrio, W., Brown, G.G., Eisenhauer, N., 2020. Climate change effects on earthworms - a review. Soil Organisms91, 114–137.
CrossRef Google scholar
[63]
Sjursen, H., Bayley, M., Holmstrup, M., 2001. Enhanced drought tolerance of a soil-dwelling springtail by pre-acclimation to a mild drought stress. Journal of Insect Physiology47, 1021–1027.
CrossRef Google scholar
[64]
Spinoni, J., Barbosa, P., Cherlet, M., Forzieri, G., McCormick, N., Naumann, G., Vogt, J.V., Dosio, A., 2021. How will the progressive global increase of arid areas affect population and land-use in the 21st century ? Global and Planetary Change 205, 103597.
[65]
Sunday, J.M., Bates, A.E., Dulvy, N.K., 2011. Global analysis of thermal tolerance and latitude in ectotherms. Proceedings of the Royal Society B: Biological Sciences278, 1823–1830.
CrossRef Google scholar
[66]
Szabó, B., Bálint, B., Balogh, K., Mézes, M., Seres, A., 2022. Changes in soil moisture and temperature modify the toxicity of sodium selenite and sodium selenate for Folsomia candida (Collembola) Willem 1902. Applied Soil Ecology177, 104543.
CrossRef Google scholar
[67]
Tabari, H., 2020. Climate change impact on flood and extreme precipitation increases with water availability. Scientific Reports10, 13768.
CrossRef Google scholar
[68]
Uhía, E., Briones, M.J.I., 2002. Population dynamics and vertical distribution of enchytraeids and tardigrades in response to deforestation. Acta Oecologica23, 349–359.
CrossRef Google scholar
[69]
van Vliet, P.C.J., West, L.T., Hendrix, P.F., Coleman, D.C., 1993. The influence of Enchytraeidae (Oligochaeta) on the soil porosity of small microcosms. In: Brussaard, L., Kooistra, M.J., eds. Soil Structure/Soil Biota Interrelationships. Amsterdam: Elsevier, 287–299.
[70]
Yusefi, G.H., Safi, K., Tarroso, P., Brito, J.C., 2021. The impacts of extreme climate change on mammals differ among functional groups at regional scale: the case of Iranian terrestrial mammals. Diversity and Distributions27, 1634–1647.
CrossRef Google scholar

Declaration of competing interest

The authors declare no competing interests.

Acknowledgements

This study was supported by the European Commission Project NANORIGO (H2020-NMBP-13-2018, GA No. 814530). Further this study was supported by BEAUTY (PTDC/CTA-AMB/3970/2020, https://doi.org/10.54499/PTDC/CTA-AMB/3970/2020) and by CESAM [UIDB/50017/2020 + UIDP/50017/2020 + LA/P/0094/2020], via Fundação para a Ciência e a Tecnologia (FCT)/ Ministério da Educação e Ciência (MEC) through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. R. Bicho is funded by FCT, I.P. via a research contract under the Scientific Employment Stimulus - Individual Call (CEEC Individual) - 2021.01725.CEECIND/CP1659/CT0003, https://doi.org/10.54499/2021.01725.CEECIND/CP1659/CT0003. Open access funding provided by FCT|FCCN (b-on).

Open access

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

RIGHTS & PERMISSIONS

2024 The Author(s) 2024. This article is published with open access at link.springer.com and journal.hep.com.cn
AI Summary AI Mindmap
PDF(1343 KB)

Accesses

Citations

Detail

Sections
Recommended

/