Abstract
Invasive species often displace native species by outcompeting them. Yet, some native species can persist even in heavily invaded areas. The mechanisms mediating this local coexistence are still unclear. Fine-scale microclimatic heterogeneity could promote the local coexistence of native and invasive animal competitors. We tested if native ant species could coexist with a recent ant invader, Tapinoma magnum, by shifting their foraging activity in time or space to different microclimatic conditions. We compared the foraging activity of native epigeic ant species among invaded and uninvaded sites. We collected ants at baits in green spaces on the north, east, south and west sides of buildings in the morning, at noon and in the afternoon to test if native species foraged under different microclimatic conditions in invaded sites. Invaded sites had lower ant species richness, diversity, and relative abundance. The native black garden ant Lasius niger – one of the most widespread Palearctic ant species – persisted at high densities in invaded areas but foraged less on the east side of buildings and more on the west side. Microclimatic heterogeneity might promote native and invasive species coexistence by allowing some native species to shift their foraging behaviour to locally avoid or outcompete invasive competitors. Better understanding how fine-scale micro-environmental heterogeneity affects native species’ persistence in invaded areas could help to predict and locally mitigate the negative impacts of biological invasions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support the findings of this study are openly available at https://github.com/JGippet/Tmagnum_impacts.
Code availability
The R code and data used to perform statistical analyses and associated figures are openly available at https://github.com/JGippet/Tmagnum_impacts.
References
Achury R, Holway DA, Suarez AV (2020) Pervasive and persistent effects of ant invasion and fragmentation on native ant assemblages. Ecology 102:e03257. https://doi.org/10.1002/ecy.3257
Albrecht M, Gotelli NJ (2001) Spatial and temporal niche partitioning in grassland ants. Oecologia 126:134–141. https://doi.org/10.1007/s004420000494
Alcaraz C, Bisazza A, García-Berthou E (2008) Salinity mediates the competitive interactions between invasive mosquitofish and an endangered fish. Oecologia 155:205–213. https://doi.org/10.1007/s00442-007-0899-4
Angulo E, Caut S, Cerdá X (2011) Scavenging in Mediterranean ecosystems : effect of the invasive Argentine ant. Biol Invasions 13:1183–1194. https://doi.org/10.1007/s10530-011-9953-6
Astorg L, Sanderson S, Côté-Gravel V et al (2020) Different refuge types dampen exotic invasion and enhance diversity at the whole ecosystem scale in a heterogeneous river system. Biol Invasions. https://doi.org/10.1007/s10530-020-02374-7
Azcárate FM, Kovacs E, Peco B (2007) Microclimatic conditions regulate surface activity in harvester ants Messor barbarus. J Insect Behav 20:315–329. https://doi.org/10.1007/s10905-007-9074-3
Balzani P, Vizzini S, Frizzi F et al (2021) Plasticity in the trophic niche of an invasive ant explains establishment success and long-term coexistence. Oikos 130:691–696. https://doi.org/10.1111/oik.08217
Berthon K (2015) How do native species respond to invaders? Mechanistic and trait-based perspectives. Biol Invasions 17:2199–2211. https://doi.org/10.1007/s10530-015-0874-7
Bestelmeyer BT, Agosti D, Alonso LE, et al (2000) Field techniques for the study of ground-dwelling ants: An overview, description, and evaluation. Ants Stand methods Meas Monit Biodivers 122–128
Brooks ME, Kristensen K, van Benthem KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336. https://doi.org/10.1890/0012-9658(2002)083[2328:CFPBAI]2.0.CO;2
Buczkowski G, Mothapo NP, Wossler TC (2018) Let them eat termites—prey-baiting provides effective control of Argentine ants, Linepithema humile, in a biodiversity hotspot. J Appl Entomol 142:504–512. https://doi.org/10.1111/jen.12501
Bujan J, Roeder KA, Yanoviak SP, Kaspari M (2020) Seasonal plasticity of thermal tolerance in ants. Ecology 101:1–6. https://doi.org/10.1002/ecy.3051
Bujan J, Charavel E, Bates OK et al (2021) Increased acclimation ability accompanies a thermal niche shift of a recent invasion. J Anim Ecol 90:483–491. https://doi.org/10.1111/1365-2656.13381
Cadotte MW, Yasui SLE, Livingstone S, MacIvor JS (2017) Are urban systems beneficial, detrimental, or indifferent for biological invasion? Biol Invasions 19:3489–3503. https://doi.org/10.1007/s10530-017-1586-y
Campbell SP, Frair JL, Gibbs JP, Rundell RJ (2015) Coexistence of the endangered, endemic Chittenango ovate amber snail (Novisuccinea chittenangoensis) and a non-native competitor. Biol Invasions 17:711–723. https://doi.org/10.1007/s10530-014-0763-5
Carval D, Cotté V, Resmond R et al (2016) Dominance in a ground-dwelling ant community of banana agroecosystem. Ecol Evol 6:8617–8631. https://doi.org/10.1002/ece3.2570
Charrier NP, Hervet C, Bonsergent C et al (2020) Invasive in the North: new latitudinal record for Argentine ants in Europe. Insectes Soc 67:331–335. https://doi.org/10.1007/s00040-020-00762-9
Cordonnier M, Blight O, Angulo E, Courchamp F (2020) The native ant Lasius niger can limit the access to resources of the invasive argentine ant. Animals 10:1–17. https://doi.org/10.3390/ani10122451
Csata E, Dussutour A (2019) Nutrient regulation in ants (Hymenoptera: Formicidae): a review. Myrmecological News 29:111–124
da Silva SS, Guimarães M (2020) The enemy within: consequences of the invasive bullfrog on native anuran populations. Biol Invasions 23:373–378. https://doi.org/10.1007/s10530-020-02385-4
Dáttilo W, MacGregor-Fors I (2021) Ant social foraging strategies along a Neotropical gradient of urbanization. Sci Rep 11:1–9. https://doi.org/10.1038/s41598-021-85538-2
Dekoninck W, Parmentier T, Seifert B (2015) First records of a supercolonial species of the Tapinoma nigerrimum complex in Belgium (Hymenoptera: Formicidae). Bull Soc R Belg Entomol 151:206–209
Fox J, Weisberg S (2019) An R Companion to Applied Regression, 3rd edn. Sage Publishing, Californa
Frizzi F, Bartalesi V, Santini G (2017) Combined effects of temperature and interspecific competition on the mortality of the invasive garden ant, Lasius neglectus: A laboratory study. J Therm Biol 65:76–81. https://doi.org/10.1016/j.jtherbio.2017.02.007
Gippet JMW, Mondy N, Diallo-Dudek J et al (2017) I’m not like everybody else: urbanization factors shaping spatial distribution of native and invasive ants are species-specific. Urban Ecosyst 20:157–169. https://doi.org/10.1007/s11252-016-0576-7
Gippet JMW, Liebhold AM, Fenn-Moltu G, Bertelsmeier C (2019) Human-mediated dispersal in insects. Curr Opin Insect Sci 35:96–102
Guénard B, Dunn RR (2010) A new (Old), invasive ant in the hardwood forests of eastern North America and its potentially widespread impacts. PLoS ONE 5:1–10. https://doi.org/10.1371/journal.pone.0011614
Guo Q, Brockway DG, Larson DL et al (2018) Improving ecological restoration to curb biotic invasion - A practical guide. Invasive Plant Sci Manag 11:163–174. https://doi.org/10.1017/inp.2018.29
Guyot V, Castagneyro B, Vialatte A et al (2015) Tree diversity limits the impact of an invasive forest pest. PLoS ONE 10:1–16. https://doi.org/10.1371/journal.pone.0136469
Hart SP, Usinowicz J, Levine JM (2017) The spatial scales of species coexistence. Nat Ecol Evol 1:1066–1073. https://doi.org/10.1038/s41559-017-0230-7
Hartig F (2018) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.2.0
Holway DA (1998) Effect of Argentine ant invasions on ground-dwelling arthropods in northern California riparian woodlands. Oecologia 116:252–258
Holway DA, Lach L, Suarez AV et al (2002a) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233
Holway DA, Suarez AV, Case TJ (2002b) Role of abiotic factors in governing susceptibility to invasion: a test with argentine ants. Ecology 83:1610–1619. https://doi.org/10.1890/0012-9658(2002)083[1610:ROAFIG]2.0.CO;2
Ibarra-isassi J, Handa IT, Arenas-Clavijo A et al (2021) Shade-growing practices lessen the impact of coffee plantations on multiple dimensions of ant diversity. J Appl Ecol. https://doi.org/10.1111/1365-2664.13842
Jackson DE, Martin SJ, Holcombe M, Ratnieks FLW (2006) Longevity and detection of persistent foraging trails in Pharaoh’s ants, Monomorium pharaonis (L.). Anim Behav 71:351–359. https://doi.org/10.1016/j.anbehav.2005.04.018
Janicki J, Narula N, Ziegler M et al (2016) Visualizing and interacting with large-volume biodiversity data using client-server web-mapping applications: the design and implementation of antmaps.org. Ecol Inform 32:185–193. https://doi.org/10.1016/j.ecoinf.2016.02.006
Kenis M, Auger-Rozenberg MA, Roques A et al (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45. https://doi.org/10.1007/s10530-008-9318-y
Lenth RV (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.3. https://CRAN.R-project.org/package=emmeans
Lou HM, Cecala KK, Ennen JR et al (2018) Interspecific interactions are conditional on temperature in an Appalachian stream salamander community. Oecologia 188:623–631. https://doi.org/10.1007/s00442-018-4228-x
Ludecke D, Makowski D, Waggoner P (2019) performance: assessment of regression models performance. R package version 0.4.2
Melbourne BA, Cornell HV, Davies KF et al (2007) Invasion in a heterogeneous world: resistance, coexistence or hostile takeover? Ecol Lett 10:77–94. https://doi.org/10.1111/j.1461-0248.2006.00987.x
Nagy C, Tartally A, Vilisics F et al (2009) Effects of the invasive garden ant, Lasius neglectus Van Loon, Boomsma & András-Falvy, 1990 (Hymenoptera: Formicidae), on arthropod assemblages: pattern analyses in the type supercolony. Myrmecological News 12:171–181
Napoli M, Massetti L, Brandani G et al (2016) Modeling tree shade effect on urban ground surface temperature. J Environ Qual 45:146–156. https://doi.org/10.2134/jeq2015.02.0097
Nielsen UN, Osler GHR, Campbell CD et al (2010) The enigma of soil animal species diversity revisited: The role of small-scale heterogeneity. PLoS ONE 5:26–28. https://doi.org/10.1371/journal.pone.0011567
Oksanen J, Blanchet FG, Friendly M, et al (2020) vegan: Community Ecology Package
Pacioglu O, Theissinger K, Alexa A et al (2020) Multifaceted implications of the competition between native and invasive crayfish: a glimmer of hope for the native’s long-term survival. Biol Invasions 22:827–842. https://doi.org/10.1007/s10530-019-02136-0
Paterson JE, Blouin-Demers G (2017) Do ectotherms partition thermal resources? We still do not know. Oecologia 183:337–345. https://doi.org/10.1007/s00442-016-3762-7
Pećarević M, Danoff-Burg J, Dunn RR (2010) Biodiversity on broadway - enigmatic diversity of the societies of ants (formicidae) on the streets of New York City. PLoS ONE 5:1–8. https://doi.org/10.1371/journal.pone.0013222
Perez A, Diamond SE (2019) Idiosyncrasies in cities: Evaluating patterns and drivers of ant biodiversity along urbanization gradients. J Urban Ecol 5:1–10. https://doi.org/10.1093/jue/juz017
Pincebourde S, Murdock CC, Vickers M, Sears MW (2016) Fine-scale microclimatic variation can shape the responses of organisms to global change in both natural and urban environments. Integr Comp Biol 56:45–61. https://doi.org/10.1093/icb/icw016
Pluess T, Cannon R, Jarošík V et al (2012) When are eradication campaigns successful? A test of common assumptions. Biol Invasions 14:1365–1378. https://doi.org/10.1007/s10530-011-0160-2
Porter SD, Savignano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095–2106
R core team (2020) R v.4.0.3: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
Rabitsch W (2011) The hitchhiker’s guide to alien ant invasions. Biocontrol 56:551–572. https://doi.org/10.1007/s10526-011-9370-x
Roeder KA, Roeder DV, Kaspari M (2018) The role of temperature in competition and persistence of an invaded ant assemblage. Ecol Entomol 43:774–781. https://doi.org/10.1111/een.12663
Ruland F, Jeschke JM (2020) How biological invasions affect animal behaviour: A global, cross-taxonomic analysis. J Anim Ecol 89:2531–2541. https://doi.org/10.1111/1365-2656.13306
Savolainen R, Vepsäläinen K (1988) A competition hierarchy among boreal ants: Impact on resource partitioning and community structure. Oikos 51:135–155
Schifani E (2019) Exotic ants (Hymenoptera, Formicidae) invading Mediterranean Europe: a brief summary over about 200 years of documented introductions. Sociobiology 66:198–208
Seifert B (2007) Die ameisen mittel- und nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, Tauer, p 368p
Seifert B, D’eustacchio D, Kaufmann B et al (2017) Four species within the supercolonial ants of the Tapinoma nigerrimum complex revealed by integrative taxonomy (Hymenoptera: Formicidae). Myrmecol News 24:123–144
Spicer ME, Stark AY, Adams BJ et al (2017) Thermal constraints on foraging of tropical canopy ants. Oecologia 183:1007–1017. https://doi.org/10.1007/s00442-017-3825-4
Stahlschmidt ZR, Johnson D (2018) Moving targets: determinants of nutritional preferences and habitat use in an urban ant community. Urban Ecosyst 21:1151–1158. https://doi.org/10.1007/s11252-018-0796-0
Stuart YE, Campbell TS, Hohenlhole PA et al (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466
Suggitt AJ, Gillingham PK, Hill JK et al (2011) Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120:1–8. https://doi.org/10.1111/j.1600-0706.2010.18270.x
Tartally A (2006) Long term expansion of a supercolony of the invasive garden ant, Lasius neglectus (Hymenoptera: Formicidae ). Myrmecologische Nachrichten 9:21–25
Thomas ML, Holway DA (2005) Condition-specific competition between invasive Argentine ants and Australian Iridomyrmex. J Anim Ecol 74:532–542. https://doi.org/10.1111/j.1365-2656.2005.00952.x
Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470. https://doi.org/10.1890/02-0626
Trigos-Peral G, Abril S, Angulo E (2021) Behavioral responses to numerical differences when two invasive ants meet: the case of Lasius neglectus and Linepithema humile. Biol Invasions 23:935–953. https://doi.org/10.1007/s10530-020-02412-4
Ugelvig LV, Drijfhout FP, Kronauer DJ et al (2008) The introduction history of invasive garden ants in Europe: integrating genetic, chemical and behavioural approaches. BMC Biol 6:11
Ujiyama S, Tsuji K (2018) Controlling invasive ant species: a theoretical strategy for efficient monitoring in the early stage of invasion. Sci Rep 8:2–10. https://doi.org/10.1038/s41598-018-26406-4
Vonshak M, Dayan T, Ionescu-Hirsh A et al (2010) The little fire ant Wasmannia auropunctata: A new invasive species in the Middle East and its impact on the local arthropod fauna. Biol Invasions 12:1825–1837. https://doi.org/10.1007/s10530-009-9593-2
Wagner HC, Arthofer W, Seifert B et al (2017) Light at the end of the tunnel: Integrative taxonomy delimits cryptic species in the i Tetramorium caespitum \i complex (Hymenoptera: Formicidae). Myrmecological News 25:95–129
Warren RJ, Reed K, Mathew A et al (2019) Release from intraspecific competition promotes dominance of a non-native invader. Biol Invasions 21:895–909. https://doi.org/10.1007/s10530-018-1868-z
Wittman SE (2014) Impacts of invasive ants on native ant communities (Hymenoptera: Formicidae). Myrmecological News 19:111–123
Wittman SE, Sanders NJ, Ellison AM et al (2010) Species interactions and thermal constraints on ant community structure. Oikos 119:551–559. https://doi.org/10.1111/j.1600-0706.2009.17792.x
Wong MKL, Tsang TPN, Lewis OT, Guénard B (2021) Trait-similarity and trait-hierarchy jointly determine fine-scale spatial associations of resident and invasive ant species. Ecography (cop) 44:1–13. https://doi.org/10.1111/ecog.05505
Wright JT, Byers JE, Koukoumaftsis LP et al (2010) Native species behaviour mitigates the impact of habitat-forming invasive seaweed. Oecologia 163:527–534. https://doi.org/10.1007/s00442-010-1608-2
Žagar A, Carretero MA, Osojnik N et al (2015) A place in the sun: interspecific interference affects thermoregulation in coexisting lizards. Behav Ecol Sociobiol 69:1127–1137. https://doi.org/10.1007/s00265-015-1927-8
Acknowledgements
This work was funded by the Swiss Canton Vaud, the Fond National Suisse, and the Programme de la Famille Sandoz—Monique de Meuron pour la relève universitaire. We thank the inhabitants of Saint-Sulpice for allowing us to sample around their buildings and M. Chalmandrier for her help on the field. We thank J. Bujan and G. Fenn-Moltu and two anonymous reviewers for helpful comments on an earlier version of the manuscript.
Funding
This work was funded by the Swiss Canton Vaud, the Fond National Suisse, and the Programme de la Famille Sandoz—Monique de Meuron pour la relève universitaire.
Author information
Authors and Affiliations
Contributions
JMWG and CB designed the study. LG carried out field sampling. LG and JMWG identified the ants. JMWG and LG carried out data processing and statistical analyses. All authors wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gippet, J.M.W., George, L. & Bertelsmeier, C. Local coexistence of native and invasive ant species is associated with micro-spatial shifts in foraging activity. Biol Invasions 24, 761–773 (2022). https://doi.org/10.1007/s10530-021-02678-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-021-02678-2