Biochar soil addition alters ant functional traits as exemplified with three species

Abstract

The response of soil microorganisms and plants in soil ecosystems to biochar is well recognised. However, biochars’ impact on large soil animal, such as ants, is inadequately understood, with only limited studies focusing on the abundance and mortality rates of some specific ant species. In this study, soil physicochemical properties, and ant community diversity and functional characteristics were compared between experimental plots with and without biochar application. No significant differences in soil (soil physicochemical properties) or ants (ant community richness, species abundance, and morphological characteristics) were observed between the two plots before biochar application. However, the biochar-treated plot soil surface temperatures, pH, and soil water content were significantly higher after 48 weeks. Biochar application promoted Cardiocondyla nuda (by 426%) and Formica japonica abundance (by 93%), but decreased Solenopsis invicta invasive ant species richness (by 54%), consistent with the fact that changes in soil properties were more beneficial to the former two species. In addition, in biochar-treated plots, F. japonica and S. invicta generally showed larger body size (18% and 6.7%), larger eyes (2.7% and 4.0%), and longer femurs (6.3% and 7.9%), which enabled them to respond better to potential barriers, such as plants. Our results highlighted that, besides species abundance and community structure, certain ant functional morphological indicators were also informative in evaluating biochar ecological implications.

Highlights

•	Biochar application enhanced soil temperature, pH, and water content.
•	Ants showed larger body size, larger eyes, and longer femurs with biochar application.
•	Biochar promoted ant richness by creating ant-preferred habitats.

Keywords

Biochar / Ant / Community structure / Functional traits / Rice straw / Species abundance

References

[1] Andersen AN. Responses of ground-foraging ant communities to three experimental fire regimes in a savanna forest of tropical Australia. Biotropica, 1991, 23: 575-585,

[2] Atkinson CJ, Fitzgerald JD, Hipps NA. Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil, 2010, 337: 1-18,

[3] Biederman LA, Harpole WS. Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. GCB Bioenergy, 2012, 5: 202-214,

[4] Blanco-Canqui H. Does biochar improve all soil ecosystem services?. GCB Bioenergy, 2020, 13: 291-304,

[5] Bolton B. . Identification guide to the ant genera of the world, 1994 Cambridge Harvard University Press

[6] Castracani C, Maienza A, Grasso DA, Genesio L, Malcevschi A, Miglietta F, Vaccari FP, Mori A. Biochar-macrofauna interplay: searching for new bioindicators. Sci Total Environ, 2015, 536: 449-456,

[7] Chen Y, Zhao C, Zhang D, Zhang S, Zeng W, Li Z. The effect of amending soils with biochar on the microhabitat preferences of Coptotermes formosanus (Blattodea: Rhinotermitidae). Ecotoxicol Environ Saf, 2022, 232: 113240,

[8] Drager KI, Rivera MD, Gibson JC, Ruzi SA, Hanisch PE, Achury R, Suarez AV. Testing the predictive value of functional traits in diverse ant communities. Ecol Evol, 2023, 13(4): e10000,

[9] Elizalde L, Arbetman M, Arnan X, Eggleton P, Leal IR, Lescano MN, Pirk GI. The ecosystem services provided by social insects: traits, management tools and knowledge gaps. Biol Rev, 2020, 95(5): 1418-1441,

[10] Feng W, Yang F, Cen R, Liu J, Qu Z, Miao Q, Chen H. Effects of straw biochar application on soil temperature, available nitrogen and growth of corn. J Environ Manag, 2021, 277: 111331,

[11] Frouz J, Jilková V. The effect of ants on soil properties and processes (Hymenoptera: Formicidae). Myrmecol News, 2008, 11: 191-199

[12] Gibb H, Parr CL. Does structural complexity determine the morphology of assemblages?. An Exper Test Three Contin PLoS One, 2013, 8: e64005,

[13] Gibb H, Stoklosa J, Warton DI, Brown AM, Andrew NR, Cunningham SA. Does morphology predict trophic position and habitat use of ant species and assemblages?. Oecologia, 2015, 177: 519-531,

[14] Gorovtsov AV, Minkina TM, Mandzhieva SS, Perelomov LV, Soja G, Zamulina IV, Rajput VD, Sushkova SN, Mohan D, Yao J. The mechanisms of biochar interactions with microorganisms in soil. Environ Geochem Hlth, 2020, 42: 2495-2518,

[15] Gruss I, Twardowski JP, Latawiec A, Medynska-Juraszek A, Krolczyk J. Risk assessment of low-temperature biochar used as soil amendment on soil mesofauna. Environ Sci Pollut R, 2019, 26: 18230-18239,

[16] He M, Xiong X, Wang L, Hou D, Bolan NS, Ok YS, Rinklebe J, Tsang DCW. A critical review on performance indicators for evaluating soil biota and soil health of biochar-amended soils. J Haz Mat, 2021, 414: 125378,

[17] Helms IJA, Ijelu SE, Wills BD, Landis DA, Haddad NM. Ant biodiversity and ecosystem services in bioenergy landscapes. Agr Ecosyst Environ, 2020, 290: 106780,

[18] Hölldobler B, Wilson EO. . The ants, 1990 Berlin, Heidelberg Springer Berlin Heidelberg,

[19] Hölldobler B, Wilson EO. Host tree selection by the neotropical ant paraponera clavata (hymenoptera formicidae). Biotropica, 1990, 22: 213-214,

[20] Ibarra-Isassi J, Handa IT, Lessard JP. Community-wide trait adaptation, but not plasticity, explains ant community structure in extreme environments. Funct Ecol, 2023, 37(1): 139-149,

[21] Jeffery S, van de Voorde TFJ, Harris WE, Mommer L, Van Groenigen JW, De Deyn GB, Ekelund F, Briones MJI, Bezemer TM. Biochar application differentially affects soil micro-, meso-macro-fauna and plant productivity within a nature restoration grassland. Soil Biol Biochem, 2022, 174,

[22] Jones DL, Rousk J, Edwards-Jones G, DeLuca TH, Murphy DV. Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol Biochem, 2012, 45: 113-124,

[23] Jouquet P, Dauber J, Lagerlöf J, Lavelle P, Lepage M. Soil invertebrates as ecosystem engineers: intended and accidental effects on soil and feedback loops. Appl Soil Ecol, 2006, 32: 153-164,

[24] Kaspari M, Weiser MD. The size–grain hypothesis and interspecific scaling in ants. Funct Ecol, 2002, 13: 530-538,

[25] Khan MB, Cui X, Jilani G, Lazzat U, Zehra A, Hamid Y, Hussain B, Tang L, Yang X, He Z. Eisenia fetida and biochar synergistically alleviate the heavy metals content during valorization of biosolids via enhancing vermicompost quality. Sci Total Environ, 2019, 684: 597-609,

[26] Lach L. Invasive ant establishment, spread, and management with changing climate. Curr Opin Insect Sci, 2021, 47: 119-124,

[27] Lieke T, Zhang X, Steinberg CEW, Pan B. Overlooked risks of biochars: persistent free radicals trigger neurotoxicity in Caenorhabditis elegans. Environ Sci Technol, 2018, 52: 7981-7987,

[28] Liu T, Yang L, Hu Z, Xue J, Lu Y, Chen X, Griffiths BS, Whalen JK, Liu M. Biochar exerts negative effects on soil fauna across multiple trophic levels in a cultivated acidic soil. Biol Fert Soils, 2020, 56: 597-606,

[29] Luo XY, Newman C, Luo Y, Zhou ZM. Comparing ant assemblages and functional groups across urban habitats and seasons in an east asia monsoon climate area. Animals (Basel), 2022, 13: 597,

[30] Mahon MB, Campbell KU, Crist TO. Effectiveness of Winkler litter extraction and pitfall traps in sampling ant communities and functional groups in a temperate forest. Environ Entomol, 2017, 46(3): 470-479,

[31] McCormack SA, Ostle N, Bardgett RD, Hopkins DW, Vanbergen AJ. Biochar in bioenergy cropping systems: impacts on soil faunal communities and linked ecosystem processes. GCB Bioenergy, 2013, 5: 81-95,

[32] Menzel R, Stürzenbaum S, Bärenwaldt A, Kulas J, Steinberg CE. Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ Sci Technol, 2005, 39: 8324-8332,

[33] Moretti M, Dias ATC, de Bello F, Altermatt F, Chown SL, Azcárate FM, Bell JR, Fournier B, Hedde M, Hortal J, Ibanez S, Öckinger E, Sousa JP, Ellers J, Berg MP, Fox C. Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits. Funct Ecol, 2016, 31: 558-567,

[34] Nie L, Bamisile BS, Li Y, Ran H, Wang S, Wang L, Xu Y. Interspecific competition predicts the potential impact of little fire ant Wasmannia auropunctata (Roger)(Hymenoptera: Formicidae) invasion on resident ants in southern China. Insect Sci, 2023, 30(5): 1518-1530,

[35] Ning D, Yang F, Xiao Q, Ran H, Xu Y. A simple and efficient method for preventing ant escape (Hymenoptera Formicidae). Myrmecol News, 2019, 29: 57-65,

[36] Ok YS, Chang SX, Gao B, Chung HJ. SMART biochar technology-a shifting paradigm towards advanced materials and healthcare research. Environ Technol Innov, 2015, 4: 206-209,

[37] Peters MK, Peisker J, Steffan-Dewenter I, Hoiss B. Morphological traits are linked to the cold performance and distribution of bees along elevational gradients. J Biogeogr, 2016, 43: 2040-2049,

[38] Quilliam RS, Glanville HC, Wade SC, Jones DL. Life in the ‘charosphere’–does biochar in agricultural soil provide a significant habitat for microorganisms?. Soil Biol Biochem, 2013, 65: 287-293,

[39] Razzaghi F, Obour PB, Arthur E. Does biochar improve soil water retention?. A System Rev Meta-Anal Geode, 2020, 361: 114055,

[40] Salas-Lopez A, Violle C, Mallia L, Orivel J, Didham R. Land-use change effects on the taxonomic and morphological trait composition of ant communities in French Guiana. Insect Conserv Diver, 2018, 11: 162-173,

[41] Schultheiss P, Nooten SS, Wang R, Wong MK, Brassard F, Guénard B. The abundance, biomass, and distribution of ants on Earth. PNAS, 2022, 119(40): e2201550119,

[42] Siddiqui JA, Bamisile BS, Khan MM, Islam W, Hafeez M, Bodlah I, Xu Y. Impact of invasive ant species on native fauna across similar habitats under global environmental changes. Environ Sci Pollut R, 2021, 28: 54362-54382,

[43] Singh H, Northup BK, Rice CW, Prasad PVV. Biochar applications influence soil physical and chemical properties, microbial diversity, and crop productivity: a meta-analysis. Biochar, 2022, 4(1): 8,

[44] Steinbeiss S, Gleixner G, Antonietti M. Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol Biochem, 2009, 41: 1301-1310,

[45] Steinberg CEW (2023) A Salmon is a salmon. Sust Aqua Res 2. https://doi.org/10.5281/zenodo.7821652

[46] Sun F, Chen J, Chen F, Wang X, Liu K, Yang Y, Tang M. Influence of biochar remediation on Eisenia fetida in Pb-contaminated soils. Chemosphere, 2022, 295: 133954,

[47] Tiede Y, Schlautmann J, Donoso DA, Wallis CIB, Bendix J, Brandl R, Farwig N. Ants as indicators of environmental change and ecosystem processes. Ecol Indic, 2017, 83: 527-537,

[48] Van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, Joseph S, Cowie A. Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil, 2009, 327: 235-246,

[49] Vasconcelos HL, Leite MF, Vilhena JMS, Lima AP, Magnusson WE. Ant diversity in an Amazonian savanna: relationship with vegetation structure, disturbance by fire, and dominant ants. Austral Ecol, 2008, 33: 221-231,

[50] Vogt JT, Arthur GA. Standard metabolic rate of the fire ant, Solenopsis invicta Buren: effects of temperature, mass, and caste. J Insect Physiol, 1999, 45: 655-666,

[51] Weiser MD, Kaspari M. Ecological morphospace of new world ants. Ecol Entomol, 2006, 31: 131-142,

[52] Weiss KCB, Ray CA. Unifying functional trait approaches to understand the assemblage of ecological communities: synthesizing taxonomic divides. Ecography, 2019, 42: 2012-2020,

[53] Wu J, Wang C. . Chinese ants, 1995 BeiJing China Forestry Publishing House

[54] Zhang X, Lu ZX, Zhang NN, Chen YQ. Data of ant community compositions and functional traits responding to land-use change at the local scale. Biodivers Data J, 2022, 10: e85119,

Funding

National Natural Science Foundation of China(42067055); Yunnan Major Scientific and Technological Projects(202202AG050019)