Abstract
Some invasive ants have worldwide distributions and impose substantial impacts on human society and native biodiversity. Yet we know little about how ants impact soil ecosystems in general, much less how soil ecosystems shift when invasive ants move in. We excavated the coarse roots of a monodominant savanna tree in invaded and uninvaded areas to test the hypothesis that the presence of invasive ants would be associated with changes in root distribution and biomass across the landscape. We found that in the presence of invasive ants, trees had a shifted distribution of lateral coarse roots, with proportionally less root biomass near the surface and far from tree stems. In addition, the density of lateral coarse-root biomass was ~ 20% lower for trees within invaded landscapes. Our results suggest that soil-nesting invasive ants can drive important changes in rooting strategy for a tree species that serves a foundational role in the biogeochemical cycles of vertisol savannas.
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All of the data and analysis for this article are available at Dryad: https://doi.org/10.5061/dryad.5x69p8d7f.
References
Adcock K (2007) Estimates of black rhino carrying capacity at Ol Pejeta’s new rhino area. Kenya Wildlife Service Rhino Program, Nairobi
Batjes NH, Sombroek WG (1997) Possibilities for carbon sequestration in tropical and subtropical soils. Glob Change Biol 3:161–173. https://doi.org/10.1046/j.1365-2486.1997.00062.x
Brooks ME, Kristensen K, van Bentham KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Cammeraat ELH, Risch AC (2008) The impact of ants on mineral soil properties and processes at different spatial scales. J Appl Entomol 132:285–294. https://doi.org/10.1111/j.1439-0418.2008.01281.x
De Almeida T, Mesléard F, Santonja M et al (2020) Above- and below-ground effects of an ecosystem engineer ant in Mediterranean dry grasslands. Proc R Soc B 287:20201840. https://doi.org/10.1098/rspb.2020.1840
de la Cruz RM (2008) Metodos para analizar datos puntuales. In: Maestre FT, Escudero A, Bonet A (eds) Introduccion al analisis espacial de datos en ecologia y ciencias ambientales: metodos y aplicaciones. Asociacion Espanola de Ecologia Terrestre, Universidad Rey Juan Carlos and Caja de Ahorros del Mediterraneo, pp 76–127
DeCarlo KF, Caylor KK (2019) Biophysical effects on soil crack morphology in a faunally active dryland vertisol. Geoderma 334:134–145
DeFauw SL, Vogt JT, Boykin DL (2008) Influence of mound construction by red and hybrid imported fire ants on soil chemical properties and turfgrass in a sod production agroecosystem. Insect Soc 55:301–312. https://doi.org/10.1007/s00040-008-1006-5
Del Toro I, Ribbons RR, Pelini SL (2012) The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol News 17:133–146
Drager KI, Hirmas DR, Hasiotis ST (2016) Effects of ant (Formica subsericea) nests on physical and hydrological properties of a fine-textured soil. Soil Sci Soc Am J 80:364–375. https://doi.org/10.2136/sssaj2015.08.0300
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80. https://doi.org/10.1146/annurev-ecolsys-102209-144650
Farji-Brener AG, Werenkraut V (2017) The effects of ant nests on soil fertility and plant performance: a meta-analysis. J Anim Ecol 86:866–877. https://doi.org/10.1111/1365-2656.12672
Fischer G, Fisher BL (2013) A revision of Pheidole Westwood (Hymenoptera: Formicidae) in the islands of the Southwest Indian Ocean and designation of a neotype for the invasive Pheidole megacephala. Zootaxa 3683:301–356
Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers Conserv 7:1221–1244
Fournier D, Tindo M, Kenne M et al (2012) Genetic structure, nestmate recognition and behaviour of two cryptic species of the invasive big-headed ant Pheidole megacephala. PLoS ONE 7:e31480. https://doi.org/10.1371/journal.pone.0031480
Fox-Dobbs K, Doak DF, Brody AK, Palmer TM (2010) Termites create spatial structure and govern ecosystem function by affecting N2 fixation in an East African savanna. Ecology 91:1296–1307
Frelich LE, Hale CM, Scheu S et al (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245. https://doi.org/10.1007/s10530-006-9019-3
Goheen JR, Palmer TM (2010) Defensive plant-ants stabilize megaherbivore-driven landscape change in an African savanna. Curr Biol 20:1768–1772. https://doi.org/10.1016/j.cub.2010.08.015
Green WP, Pettry DE, Switzer RE (1998) Formicarious pedons, the initial effect of mound-building ants on soils. Soil Surv Horizons 39:33–44
Hays BR, Riginos C, Palmer TM et al (2022) Demographic consequences of mutualism disruption: browsing and big-headed ant invasion drive acacia population declines. Ecology 103:e3655
Hoffmann BD (1998) The big-headed Ant Pheidole megacephala: a new threat to monsoonal northwestern Australia. Pac Conserv Biol 4:250–255. https://doi.org/10.1071/PC980250
Holway DA, Lach L, Suarez AV et al (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233. https://doi.org/10.1146/annurev.ecolsys.33.010802.150444
Jackson RB, Lajtha K, Crow SE et al (2017) The ecology of soil carbon: pools, vulnerabilities, and biotic and abiotic controls. Annu Rev Ecol Evol Syst 48:419–445. https://doi.org/10.1146/annurev-ecolsys-112414-054234
Kidanu S, Mamo T, Stroosnijder L (2005) Biomass production of Eucalyptus boundary plantations and their effect on crop productivity on Ethiopian highland Vertisols. Agrofor Syst 63:281–290
Kristensen JA, Svenning J-C, Georgiou K, Malhi Y (2021) Can large herbivores enhance ecosystem carbon persistence? Trends Ecol Evol 37:117–128. https://doi.org/10.1016/j.tree.2021.09.006
Krushelnycky PD, Gillespie RG (2010) Sampling across space and time to validate natural experiments: an example with ant invasions in Hawaii. Biol Invasions 12:643–655. https://doi.org/10.1007/s10530-009-9471-y
Kueffer C, Pyšek P, Richardson DM (2013) Integrative invasion science: model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytol 200:615–633. https://doi.org/10.1111/nph.12415
Kumschick S, Gaertner M, Vilà M et al (2015) Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience 65:55–63. https://doi.org/10.1093/biosci/biu193
Lafleur B, Hooper-Bùi LM, Paul Mumma E, Geaghan JP (2005) Soil fertility and plant growth in soils from pine forests and plantations: Effect of invasive red imported fire ants Solenopsis invicta (Buren). Pedobiologia 49:415–423. https://doi.org/10.1016/j.pedobi.2005.05.002
Lambers H, Chapin FS, Pons TL (2008) Plant physiological ecology. Springer
Lavelle P, Spain A, Fonte S et al (2020) Soil aggregation, ecosystem engineers and the C cycle. Acta Oecol 105:103561. https://doi.org/10.1016/j.actao.2020.103561
Leite PAM, Carvalho MC, Wilcox BP (2018) Good ant, bad ant? Soil engineering by ants in the Brazilian Caatinga differs by species. Geoderma 323:65–73. https://doi.org/10.1016/j.geoderma.2018.02.040
Lubbers IM, van Groenigen KJ, Fonte SJ et al (2013) Greenhouse-gas emissions from soils increased by earthworms. Nat Clim Change 3:187–194. https://doi.org/10.1038/nclimate1692
Mekonnen K, Yohannes T, Glatzel G, Amha Y (2006) Performance of eight tree species in the highland Vertisols of central Ethiopia: growth, foliage nutrient concentration and effect on soil chemical properties. New for 32:285–298
Milligan PD, Prior KM, Palmer TM (2016) An invasive ant reduces diversity but does not disrupt a key ecosystem function in an African savanna. Ecosphere 7:e01502. https://doi.org/10.1002/ecs2.1502
Milligan PD, Martin TA, John GP et al (2021) Mutualism disruption by an invasive ant reduces carbon fixation for a foundational East African ant-plant. Ecol Lett 24:1052–1062
Milligan PD, Martin TA, Pringle EG et al (2022) A soil-nesting invasive ant disrupts carbon dynamics in saplings of a foundational ant–plant. J Ecol 110:359–373
Miranda JC, Rodríguez-Calcerrada J, Pita P et al (2020) Carbohydrate dynamics in a resprouting species after severe aboveground perturbations. Eur J for Res 139:841–852. https://doi.org/10.1007/s10342-020-01288-2
Moser JC (2006) Complete excavation and mapping of a Texas leafcutting ant nest. Ann Entomol Soc Am 99:891–897. https://doi.org/10.1603/0013-8746(2006)99[891:CEAMOA]2.0.CO;2
Moutinho P, Nepstad DC, Davidson EA (2003) Influence of leaf-cutting ant nests on secondary forest growth and soil properties in Amazonia. Ecology 84:1265–1276. https://doi.org/10.1890/0012-9658(2003)084[1265:IOLANO]2.0.CO;2
Nkem JN, Lobry de Bruyn LA, Grant CD, Hulugalle NR (2000) The impact of ant bioturbation and foraging activities on surrounding soil properties. Pedobiologia 44:609–621. https://doi.org/10.1078/S0031-4056(04)70075-X
Palmer TM, Riginos C, Milligan PD et al (2021) Frenemy at the gate: Invasion by Pheidole megacephala facilitates a competitively subordinate plant ant in Kenya. Ecology 102:e03230. https://doi.org/10.1002/ecy.3230
Pietrek AG, Goheen JR, Riginos C et al (2021) Density dependence and the spread of invasive big-headed ants (Pheidole megacephala) in an East African savanna. Oecologia 195:667–676. https://doi.org/10.1007/s00442-021-04859-1
Riginos C, Grace JB (2008) Savanna tree density, herbivores, and the herbaceous community: bottom-up vs. top-down effects. Ecology 89:2228–2238. https://doi.org/10.1890/07-1250.1
Riginos C, Grace JB, Augustine DJ, Young TP (2009) Local versus landscape-scale effects of savanna trees on grasses. J Ecol 97:1337–1345
Riginos C, Karande MA, Rubenstein DI, Palmer TM (2015) Disruption of a protective ant–plant mutualism by an invasive ant increases elephant damage to savanna trees. Ecology 96:654–661. https://doi.org/10.1890/14-1348.1
Rousset F, Ferdy J-B (2014) Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography 37:781–790. https://doi.org/10.1111/ecog.00566
Schultheiss P, Nooten SS, Wang R et al (2022) The abundance, biomass, and distribution of ants on Earth. Proc Natl Acad Sci 119:e2201550119
Shatters RG, Vander Meer RK (2000) Characterizing the interaction between fire ants (Hymenoptera: Formicidae) and developing soybean plants. J Econ Entomol 93:1680–1687. https://doi.org/10.1603/0022-0493-93.6.1680
Shukla RK, Singh H, Rastogi N, Agarwal VM (2013) Impact of abundant Pheidole ant species on soil nutrients in relation to the food biology of the species. Appl Soil Ecol 71:15–23. https://doi.org/10.1016/j.apsoil.2013.05.002
Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268. https://doi.org/10.1007/s10530-011-9956-3
Smith MG, Arndt SK, Miller RE et al (2018) Trees use more non-structural carbohydrate reserves during epicormic than basal resprouting. Tree Physiol 38:1779–1791. https://doi.org/10.1093/treephys/tpy099
Springett J, Gray R (1997) The interaction between plant roots and earthworm burrows in pasture. Soil Biol Biochem 29:621–625. https://doi.org/10.1016/S0038-0717(96)00235-0
Syrjala SE (1996) A statistical test for a difference between the spatial distributions of two populations. Ecology 77:75–80. https://doi.org/10.2307/2265656
Wang S, Li J, Zhang Z et al (2019) Feeding-strategy effect of Pheidole ants on microbial carbon and physicochemical properties in tropical forest soils. Appl Soil Ecol 133:177–185. https://doi.org/10.1016/j.apsoil.2018.10.006
Wardle DA, Bellingham PJ, Fukami T, Mulder CPH (2007) Promotion of ecosystem carbon sequestration by invasive predators. Biol Lett 3:479–482. https://doi.org/10.1098/rsbl.2007.0163
Wetterer JK (2012) Worldwide spread of the African big-headed ant, Pheidole megacephala (Hymenoptera: Formicidae). Myrmecol News 17:51–62
Wigley BJ, Staver AC, Zytkowiak R et al (2019) Root trait variation in African savannas. Plant Soil 441:555–565. https://doi.org/10.1007/s11104-019-04145-3
Wilson EO, Hölldobler B (2005) The rise of the ants: a phylogenetic and ecological explanation. PNAS 102:7411–7414. https://doi.org/10.1073/pnas.0502264102
Young TP, Stubblefield CH, Isbell LA (1997) Ants on swollen-thorn acacias: species coexistence in a simple system. Oecologia 109:98–107. https://doi.org/10.1007/s004420050063
Zhong Z, Li X, Sanders D et al (2021) Soil engineering by ants facilitates plant compensation for large herbivore removal of aboveground biomass. Ecology 102:e03312. https://doi.org/10.1002/ecy.3312
Zhou Y, Wigley BJ, Case MF et al (2020) Rooting depth as a key woody functional trait in savannas. New Phytol 227:1350–1361. https://doi.org/10.1111/nph.16613
Broekhuysen GJ (1947) The Brown House Ant (Pheidole megacephala, Fabr.) in South Africa. Bull Dep Agric S Afr 1–40
R Core Team (2021) R: a language and environment for statistical computing
Acknowledgements
We thank the Kenyan government (NACOSTI/P/20/3255) for their permission to conduct this project and the National Museums of Kenya for supporting it. The Mpala Research Centre and the Ol Pejeta Conservancy provided logistical support, with special thanks to Nelly Maiyo and Stephen Kesiyo. This work was supported by grants from the U.S. National Science Foundation to EGP (NSF DEB-1935498), PDM (NSF PRFB-2010075), and TMP (NSF DEB-1556905). The authors have no relevant financial or non-financial interests to disclose.
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EP and TP conceived and designed the study with support from SM, BG, and AK. JL, JM, and PM conducted the experiments and measurements. PM and EP analyzed the data. EP, PM, and TP wrote the manuscript.
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Milligan, P.D., Palmer, T.M., Lemboi, J.S. et al. Ant invasion is associated with lower root density and different root distribution of a foundational savanna tree species. Biol Invasions 25, 1683–1691 (2023). https://doi.org/10.1007/s10530-023-03008-4
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DOI: https://doi.org/10.1007/s10530-023-03008-4