Research advances in trait-based approaches in soil animal community ecology

doi:10.13287/j.1001-9332.202404.028

Abstract

Abstract: Functional traits are indicators of the responses and adaptation of organisms to environmental changes and cascade to a series of ecosystem functions. The functional traits of soil animals are sensitive to environmental factors and may characterize and predict the changes of ecosystem functions. Multiple dimensions of biodiversity that combing species, phylogenetic, and functional diversity improves the understanding of distribution patterns, community assembly mechanisms and ecosystem functions of soil animals. In this review, we listed the categories of soil animal functional traits and their ecological significance, and summarized current researches on the responses of soil animal communities to environmental changes and the community assembly processes based on trait-based approaches. We proposed to strengthen the study on the impacts of eco-evolution processes of biotic interactions to soil animal functional traits, establish the database of soil animal functional traits, and apply trait-based approaches in the ecological restoration in the future, which would benefit soil biodiversity conservation and sustainability of soil ecosystems.

Key words: biodiversity, functional trait, soil animal, functional diversity, community assembly

SUN Xin, XIE Zhijing, QIAO Zhihong, GAO Meixiang, YIN Rui, CHANG Liang, WU Donghui, LIU Manqiang, ZHU Yongguan. Research advances in trait-based approaches in soil animal community ecology[J]. Chinese Journal of Applied Ecology, 2024, 35(4): 1150-1158.

References

[1] Violle C, Navas ML, Vile D, et al. Let the concept of trait be functional! Oikos, 2007, 116: 882-892
[2] Pey B, Laporte B, Hedde M. nBETSI database tutorial [EB/OL]. (2014-10-18)[2023-02-17]. https://portail.betsi.cnrs.fr/node/2
[3] Vandewalle M , Bello FD , Berg MP, et al. Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiversity and Conservation, 2010, 19: 2921-2947
[4] Ferrín M, Márquez L, Petersen H, et al. Trait-mediated responses to aridity and experimental drought by springtail communities across Europe. Functional Ecology, 2023, 37: 44-56
[5] 孟凡凡, 胡盎, 王建军. 微生物性状揭示物种分布格局、群落构建机制和生态系统功能. 微生物学报, 2020, 60(9): 1784-1800
[6] 孙新, 李琪, 姚海凤, 等. 土壤动物与土壤健康. 土壤学报, 2021, 58(5): 1073-1083
[7] Moretti M, Dias AT, de Bello F, et al. Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits. Functional Ecology, 2017, 31: 558-567
[8] Salmon S, Ponge JF, Gachet S, et al. Linking species, traits and habitat characteristics of Collembola at European scale. Soil Biology and Biochemistry, 2014, 75: 73-85
[9] Andriuzzi WS, Franco ALC, Ankrom KE, et al. Body size structure of soil fauna along geographic and temporal gradients of precipitation in grasslands. Soil Biology and Biochemistry, 2020, 140: 107638
[10] Thakur MP, Siguresson BD, Siguresson P, et al. Warming shifts the biomass distribution of soil microarthropod communities. Soil Biology and Biochemistry, 2023, 177: 108894
[11] Malcicka M, Berg MP, Ellers J. Ecomorphological adaptations in Collembola in relation to feeding strategies and microhabitat. European Journal of Soil Biology, 2017, 78: 82e91
[12] Yin R, Kardol P, Thakur MP, et al. Soil functional biodiversity and biological quality under threat: Intensive land use outweighs climate change. Soil Biology and Biochemistry, 2020, 147: 107847
[13] Qiao ZH, Wang B, Yao HF, et al. Urbanization and greenspace type as determinants of species and functional composition of collembolan communities. Geoderma, 2022, 428: 116175
[14] Law SJ, Bishop TR, Eggleton P, et al. Darker ants dominate the canopy: Testing macroecological hypotheses for patterns in colour along a microclimatic gradient. Journal of Animal Ecology, 2020, 89: 347-359
[15] Yeates GW, Bongers T, De Goede RG, et al. Feeding habits in soil nematode families and genera: An outline for soil ecologists. Journal of Nematology, 1993, 25: 315-331
[16] Holmstrup M, Ehlers BK, Slotsbo S, et al. Functional diversity of Collembola is reduced in soils subjected to short-term, but not long-term, geothermal warming. Functional Ecology, 2018, 32: 1304-1316
[17] Coq S, Ganault P, Mer GL, et al. Faeces traits as uni-fying predictors of detritivore effects on organic matter turnover. Geoderma, 2022, 422: 115940
[18] Ellers J, Berg MP, Dias ATC, et al. Diversity in form and function: Vertical distribution of soil fauna mediates multidimensional trait variation. Journal of Animal Eco-logy, 2018, 87: 933-944
[19] Diaz AT, Krab EJ, Marien J, et al. Traits underpinning desiccation resistance explain distribution patterns of terrestrial isopods. Oecologia, 2013, 172: 667-677
[20] Verdu JR, Casas JL, Lobo JM, et al. Dung beetles eat acorns to increase their ovarian development and thermal tolerance. PLoS One, 2010, 5: e10114
[21] Andriuzzi WS, Wall DH. Grazing and resource availabi-lity control soil nematode body size and abundance-mass relationship in semi-arid grassland. Journal of Animal Ecology, 2018, 87: 1407-1417
[22] Ferris H. Contribution of nematodes to the structure and function of the soil food web. Journal of Nematology, 2010, 42: 63-67
[23] Santorufo L, Cortet J, Arena C, et al. An assessment of the influence of the urban environment on collembolan communities in soils using taxonomy- and trait-based approaches. Applied Soil Ecology, 2014, 78: 48-56
[24] Joimel S, Schwartz C, Maurel N, et al. Contrasting homogenization patterns of plant and collembolan communities in urban vegetable gardens. Urban Ecosystems, 2019, 22: 553-566
[25] Pan SF, Liang J, Wu HB, et al. Effect of urban gree-ning and afforestation on soil microarthropod communities in coastal reclaimed land: Insights from functional traits. Applied Soil Ecology, 2022, 173: 104391
[26] Fournier B, Frey D, Moretti M. The origin of urban communities: From the regional species pool to community assemblages in city. Journal of Biogeography, 2020, 47: 615-629
[27] Parr CL, Dunn RR, Sanders NJ, et al. GlobalAnts: A new database on the geography of ant traits (Hymenoptera: Formicidae). Insect Conservation and Diversity, 2017, 10: 5-20
[28] Piano E, Souffreau C, Merckx T. et al. Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales. Global Change Biology, 2020, 26: 1196-1211
[29] Kȩdzior R, Szwalec A, Mundała P, et al. Ground beetle (Coleoptera, Carabidae) life history traits as indicators of habitat recovering processes in postindustrial areas. Ecological Engineering, 2020, 142: 105615
[30] Zhang AJ, Zhang Y, Potapov AM, et al. Changes in diversity and functional groups of soil mite communities are associated with properties of food resources along a subalpine secondary succession. Geoderma, 2023, 432: 116395
[31] Sun X, Deharveng L, Bedos A, et al. Changes in diversity and body size of Onychiurinae (Collembola: Onychiuridae) along an altitudinal gradient in Changbai Mountain, China. Soil Ecology Letters, 2020, 2: 230-239
[32] Pan X, Xie ZJ, Sun X, et al. Changes in oribatid mite community structure along two altitudinal gradients in Asia and Europe as related to environmental factors. Applied Soil Ecology, 2023, 189: 104912
[33] Huebner K, Lindo Z, Lechowicz MJ. Post-fire succession of collembolan communities in a northern hardwood forest. European Journal of Soil Biology, 2012, 48: 59-65
[34] Potapov AM, Guerra CA, van den Hoogen J, et al. Globally invariant metabolism but density-diversity mismatch in springtails. Nature Communications, 2023, 14: 674
[35] Huang N, Wang L, Song XP, et al. Spatial and temporal variations in global soil respiration and their relationships with climate and land cover. Science Advances, 2020, 6: eabb8508
[36] Yin R, Qin W, Wang X, et al. Experimental warming causes mismatches in alpine plant-microbe-fauna pheno-logy. Nature Communications, 2023, 14: 2159
[37] Potapov AM, Dupérré N, Jochum M, et al. Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change. Ecology, 2020, 101: e02957
[38] 刘任涛, 朱凡, 贺达汉, 等. 草地开垦对土壤动物多样性与功能群结构的影响.中国草地学报, 2014, 36(6): 34-40
[39] Knop E. Biotic homogenization of three insect groups due to urbanization. Global Change Biology, 2016, 22: 228-236
[40] Grimm NB, Faeth SH, Golubiewski NE, et al. Global change and the ecology of cities. Science, 2008, 319: 756-760
[41] Groffman PM, Avolio M, Cavender-Bares J, et al. Ecological homogenization of residential macrosystems. Nature Ecology Evolution, 2017, 1: 0191
[42] Tóth Z, Hornung E. Taxonomic and functional response of Millipedes (Diplopoda) to urban soil disturbance in a Metropolitan area. Insects, 2020, 11: 25
[43] Dahirel M, Dierick J, De Cock M, et al. Intraspecific variation shapes community-level behavioral responses to urbanization in spiders. Ecology, 2017, 98: 2379-2390
[44] Milano V, Cortet J, Baldantoni D, et al. Collembolan biodiversity in Mediterranean urban parks: Impact of history, urbanization, management and soil characteristics. Applied Soil Ecology, 2017, 119: 428-437
[45] Ooms A, Dias ATC, van Oosten AR, et al. Species richness and functional diversity of isopod communities vary across an urbanisation gradient, but the direction and strength depend on soil type. Soil Biology and Biochemistry, 2020, 148: 107851
[46] Barbaro L, Halder IV. Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes. Ecography, 2009, 32: 321-333
[47] Rousseau L, Venier L, Aubin I, et al. Woody biomass removal in harvested boreal forest leads to a partial functional homogenization of soil mesofaunal communities relative to unharvested forest. Soil Biology and Bioche-mistry, 2019, 133: 129-136
[48] Farská J, Prejzková K, Rusek J. Management intensity affects traits of soil microarthropod community in montane spruce forest. Applied Soil Ecology, 2014, 75: 71-79
[49] Yin R, Siebert J, Eisenhauer N, et al. Climate change and intensive land use reduce soil animal biomass via dissimilar pathways. eLife, 2020, 9: e54749
[50] Barber NA, Lamagdeleine-Dent KA, Willand JE, et al. Species and functional trait re-assembly of ground beetle communities in restored grasslands. Biodiversity and Conservation, 2017, 26: 3481-3498
[51] Liu T, Guo R, Ran W, et al. Body size is a sensitive trait-based indicator of soil nematode community response to fertilization in rice and wheat agroecosystems. Soil Biology and Biochemistry, 2015, 88: 275-281
[52] Vazquez C, de Goede RGM, Korthals GW, et al. The effects of increasing land use intensity on soil nematodes: A turn towards specialism. Functional Ecology, 2019, 33: 2003-2016
[53] Gong X, Chen X, Geisen S, et al. Agricultural habitats are dominated by rapidly evolving nematodes revealed through phylogenetic comparative methods. Soil Biology and Biochemistry, 2021, 155: 108183
[54] Yu DY, Yao J, Chen XY, et al. Ecological intensification alters the trait-based responses of soil microarthropods to extreme precipitation in agroecosystem. Geoderma, 2022, 422: 115956
[55] Chassain J, Joimel S, Gonod LV. Collembola taxonomic and functional diversity in conventional, organic and conservation cropping systems. European Journal of Soil Biology, 2023, 118: 103530
[56] Harrington R, Anton C, Dawson TP, et al. Ecosystem services and biodiversity conservation: Concepts and a glossary. Biodiversity and Conservation, 2010, 19: 2773-2790
[57] Wright JP, Naeem S, Hector A, et al. Conventional functional classification schemes underestimate the relationship with ecosystem functioning. Ecology Letters, 2006, 9: 111-120
[58] Díaz S, Lavorel S, de Bello F, et al. Incorporating plant functional diversity effects in ecosystem service assessments. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104: 20684-20689
[59] Gagic V, Bartomeus I, Jonsson T, et al. Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Procee-dings of the Royal Society B: Biological Sciences, 2015, 282: 20142620
[60] 王宇彤, 牛克昌. 青藏高原高寒草甸土壤环境对线虫功能多样性的影响. 生物多样性, 2020, 28(6): 707-717
[61] Joimel S, Schwartz C, Bonfanti J, et al. Functional and taxonomic diversity of Collembola as complementary tools to assess land use effects on soils biodiversity. Frontiers in Ecology and Evolution, 2021, 9: 630919
[62] Mori AS, Ota AT, Fujii S, et al. Concordance and discordance between taxonomic and functional homogenization: Responses of soil mite assemblages to forest conversion. Oecologia, 2015, 179: 527-535
[63] Nunes CA, Braga RF, Figueira JEC, et al. Dung beetles along a tropical altitudinal gradient: Environmental filtering on taxonomic and functional diversity. PLoS One, 2016, 11: e0157442
[64] 高梅香, 林琳, 常亮, 等. 土壤动物群落空间格局和构建机制研究进展. 生物多样性, 2018, 26(10): 1034-1050
[65] 王少鹏, 罗明宇, 冯彦皓, 等. 生物多样性理论最新进展. 生物多样性, 2022, 30(10): 25-37
[66] Luan L, Jiang Y, Cheng M, et al. Organism body size structures the soil microbial and nematode community assembly at a continental and global scale. Nature Communications, 2020, 11: 6406
[67] Isabwe A, Yao H, Zhang S, et al. Spatial assortment of soil organisms supports the size-plasticity hypothesis. ISME Communications, 2022, 2: 102
[68] Pequeno PACL, Franklin E, Norton RA. Modelling selection, drift, dispersal and their interactions in the community assembly of Amazonian soil mites. Oecologia, 2021, 196: 805-814
[69] Widenfalk LA, Malmström A, Berg MP, et al. Small-scale Collembola community composition in a pine forest soil: Overdispersion in functional traits indicates the importance of species interactions. Soil Biology and Biochemistry, 2016, 103: 52-62
[70] 王晓芳, 马红彬, 刘杰, 等. 放牧对草原植物功能性状影响研究进展. 应用生态学报, 2022, 33(2): 569-576
[71] 宋贤冲, 王会利, 秦文弟, 等. 退化人工林不同恢复类型对土壤微生物群落功能多样性的影响. 应用生态学报, 2019, 30(3): 841-848
[72] 傅声雷, 刘满强, 张卫信, 等. 土壤动物多样性的地理分布及其生态功能研究进展. 生物多样性, 2022, 30(10): 150-167
[73] 张卫信, 申智锋, 宋博, 等. 土壤食物网调控及其生态功能研究的困境与思考. 科技导报, 2022, 40(3): 52-63
[74] Xie ZJ, Chen TW, Potapov AM, et al. Ecological and evolutionary processes shape below-ground springtail communities along an elevational gradient. Journal of Biogeography, 2022, 49: 469-482
[75] Schaefer I, Caruso T. Oribatid mites show that soil food web complexity and close aboveground-belowground linkages emerged in the early Paleozoic. Communications Biology, 2019, 2: 387
[76] He NP, Li Y, Liu CC, et al. Plant trait networks: Improved resolution of the dimensionality of adaptation. Trends in Ecology and Evolution, 2020, 35: 908-918
[77] Auclerc A, Beaumelle L, Barantal S, et al. Fostering the use of soil invertebrate traits to restore ecosystem functioning. Geoderma, 2022, 424: 116019