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
Impacts of climate change – simulated flooding and drought events – on terrestrial invertebrates (Enchytraeids and Collembolans)
● 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 .
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.
climate change / soil moisture / phenotypic plasticity / biodiversity / ecosystem services
[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.,
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,
|
[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
|
/
〈 | 〉 |