Skip to main content
Log in

Urban colonies are more resistant to a trace metal than their forest counterparts in the ant Temnothorax nylanderi

  • Published:
Urban Ecosystems Aims and scope Submit manuscript

Abstract

Cities can be used as in situ replicates to assess the responses of organisms to environmental changes, such as increased heat or pollution. Community-level studies and more rarely population-level studies have been conducted, but they are not often based on multiple city replicates, thus preventing generalization. Our study tested whether colonies of the ant Temnothorax nylanderi from forest and urban populations exhibit distinct responses to pollution. Because this is a social species, we could also test whether social traits (colony size and mean size of adult workers) affected the response of colonies to urbanization. We collected colonies from four pairs of forest and urban habitats and reared them in the laboratory under normal or cadmium-supplemented diets. We then measured the emergence rate and size of newly-produced workers as well as the mortality rate of adult workers. In all four forest/city replicates, urban colonies were less negatively affected by cadmium than forest colonies for emergence rate and size of newly-produced workers, but not for mortality rate of adult workers. We did not find any correlation between social traits and cadmium resistance, in contrast with what was found in other eusocial insects. We discuss the potential adaptive nature of this differential response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdel-Lateif HM, Donker MH, Straalen NMV (1998) Interaction between temperature and cadmium toxicity in the isopod Porcellio scaber. Funct Ecol 12:521–527

    Google Scholar 

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ Biophotonics Int 11:36–42

    Google Scholar 

  • Alexandre CV, Esteves KE, de Moura e Mello, M.A.M. (2010) Analysis of fish communities along a rural–urban gradient in a neotropical stream (Piracicaba River Basin, São Paulo, Brazil). Hydrobiologia 641:97–114

    CAS  Google Scholar 

  • Andrewartha HG (1952) Diapause in Relation to the Ecology of Insects. Biol Rev 27:50–107

    Google Scholar 

  • Angilletta MJ, Wilson RS, Niehaus AC, Sears MW, Navas CA, Ribeiro PL (2007) Urban physiology: city ants possess high heat tolerance. PLoS ONE 2:e258

    PubMed  PubMed Central  Google Scholar 

  • Billick I, Carter C (2007) Testing the importance of the distribution of worker sizes to colony performance in the ant species Formica obscuripes Forel. Insectes Soc 54:113–117

    Google Scholar 

  • Blair RB (2001) Birds and butterflies along urban gradients in two ecoregions of the United States: is urbanization creating a homogeneous fauna? In: Lockwood JL, McKinney ML (eds) Biotic homogenization. Springer US, Boston, pp 33–56

    Google Scholar 

  • Bornstein RD (1968) Observations of the urban heat island effect in New York City. J Appl Meteorol 7:575–582

    Google Scholar 

  • Bozhkov A, Vladimir Padalko V, Dlubovskaya V, Menzianova N (2010) Resistance to heavy metal toxicity in organisms under chronic exposure. IJEB Vol4807 July 2010

  • Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102

    PubMed  Google Scholar 

  • Buczkowski G, Richmond DS (2012) The effect of urbanization on ant abundance and diversity: a temporal examination of factors affecting biodiversity. PLoS ONE 7:e41729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cervera A, Maymó AC, Sendra M, Martínez-Pardo R, Garcerá MD (2004) Cadmium effects on development and reproduction of Oncopeltus fasciatus (Heteroptera: Lygaeidae). J Insect Physiol 50:737–749

    CAS  PubMed  Google Scholar 

  • Chamberlain DE, Cannon AR, Toms MP, Leech DI, Hatchwell BJ, Gaston KJ (2009) Avian productivity in urban landscapes: a review and meta-analysis. Ibis 151:1–18

    Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Google Scholar 

  • Cheptou P-O, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci 105:3796–3799

    CAS  PubMed  Google Scholar 

  • Chick LD, Strickler SA, Perez A, Martin RA, Diamond SE (2019) Urban heat islands advance the timing of reproduction in a social insect. J Therm Biol 80:119–125

    PubMed  Google Scholar 

  • Clergeau P, Savard J-PL, Mennechez G, Falardeau G (1998) Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents. The Condor 100:413–425

    Google Scholar 

  • Crall JD, de Bivort BL, Dey B, Ford Versypt AN (2019)Social buffering of pesticides in bumblebees: agent-based modeling of the effects of colony size and neonicotinoid exposure on behavior within nests.Front Ecol Evol 7

  • Demenesku J, Mirkov I, Ninkov M, Popov Aleksandrov A, Zolotarevski L, Kataranovski D, Kataranovski M (2014) Acute cadmium administration to rats exerts both immunosuppressive and proinflammatory effects in spleen. Toxicology 326:96–108

    CAS  PubMed  Google Scholar 

  • den Besten PJ, Herwig HJ, Zandee DI, Voogt PA (1989) Effects of cadmium and PCBs on reproduction of the sea star Asterias rubens: aberrations in the early development. Ecotoxicol Environ Saf 18:173–180

    Google Scholar 

  • Diamond SE, Chick L, Perez A, Strickler SA, Martin RA (2017) Rapid evolution of ant thermal tolerance across an urban-rural temperature cline. Biol J Linn Soc 121:248–257

    Google Scholar 

  • Diamond SE, Chick LD, Perez A, Strickler SA, Zhao C (2018)Evolution of plasticity in the city: urban acorn ants can better tolerate more rapid increases in environmental temperature.Conserv Physiol 6

  • Díaz-Raviña M, Bååth E, Frostegård Å (1994) Multiple heavy metal tolerance of soil bacterial communities and its measurement by a thymidine incorporation technique. Appl Environ Microbiol 60:2238–2247

    PubMed  PubMed Central  Google Scholar 

  • Dominoni DM, Helm B, Lehmann M, Dowse HB, Partecke J (2013) Clocks for the city: circadian differences between forest and city songbirds. Proc R Soc B Biol Sci 280:20130593

    CAS  Google Scholar 

  • Evans KL, Newton J, Gaston KJ, Sharp SP, McGowan A, Hatchwell BJ (2012) Colonisation of urban environments is associated with reduced migratory behaviour, facilitating divergence from ancestral populations. Oikos 121:634–640

    Google Scholar 

  • Farji-Brener AG, Lescano N, Ghermandi L (2010) Ecological engineering by a native leaf-cutting ant increases the performance of exotic plant species. Oecologia 163:163–169

    PubMed  Google Scholar 

  • Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9:367–375

    Google Scholar 

  • Foti L, Dubs F, Gignoux J, Lata J-C, Lerch TZ, Mathieu J, Nold F, Nunan N, Raynaud X, Abbadie L et al (2017) Trace element concentrations along a gradient of urban pressure in forest and lawn soils of the Paris region (France). Sci Total Environ 598:938–948

    CAS  PubMed  Google Scholar 

  • Germaine SS, Wakeling BF (2001) Lizard species distributions and habitat occupation along an urban gradient in Tucson, Arizona. USA Biol Conserv 97:229–237

    Google Scholar 

  • Gomot A (1998) Toxic effects of cadmium on reproduction, development, and hatching in the freshwater snaillymnaea stagnalisfor water quality monitoring. Ecotoxicol Environ Saf 41:288–297

    CAS  PubMed  Google Scholar 

  • Grześ IM (2010a) Ants and heavy metal pollution – a review. Eur J Soil Biol 46:350–355

    Google Scholar 

  • Grześ IM (2010b) Zinc tolerance in the ant species Myrmica rubra originating from a metal pollution gradient. Eur J Soil Biol 46:87–90

    Google Scholar 

  • Guxens M, Sunyer J (2012) A review of epidemiological studies on neuropsychological effects of air pollution. Swiss Med Wkly 141:w13322

    PubMed  Google Scholar 

  • Heinze J, Foitzik S, Hippert A, Hölldobler B (2010) Apparent dear-enemy phenomenon and environment-based recognition cues in the ant Leptothorax nylanderi. Ethology 102:510–522

    Google Scholar 

  • Herrmann JD, Haddad NM, Levey DJ (2018) Mean body size predicts colony performance in the common eastern bumble bee (Bombus impatiens). Ecol Entomol 43:458–462

    Google Scholar 

  • Ieradi LA, Cristaldi M, Mascanzoni D, Cardarelli E, Grossi R, Campanella L (1996) Genetic damage in urban mice exposed to traffic pollution. Environ Pollut 92:323–328

    CAS  PubMed  Google Scholar 

  • Isaksson C (2010) Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth 7:342–350

    PubMed  Google Scholar 

  • Jandt JM, Dornhaus A (2014) Bumblebee response thresholds and body size: does worker diversity increase colony performance? Anim Behav 87:97–106

    Google Scholar 

  • Janssens TKS, Roelofs D, Straalen NMV (2009) Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Sci 16:3–18

    CAS  Google Scholar 

  • Johnson MTJ, Prashad CM, Lavoignat M, Saini Hargurdeep S (2018) Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proc R Soc B Biol Sci 285:20181019

    Google Scholar 

  • Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632

    Google Scholar 

  • Khimoun A, Doums C, Molet M, Kaufmann B, Peronnet R, Eyer PA, Mona S (2020) Urbanization without isolation: the absence of genetic structure among cities and forests in the tiny acorn ant Temnothorax nylanderi. Biol Lett 16:20190741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kipyatkov VE, Lopatina EB (2009) Temperature and photoperiodic control of diapase induction in the ant Lepisiota semenovi (Hymenoptera, formicidae) from Turkmenistan. J Evol Biochem Physiol 45:238–245

    Google Scholar 

  • Klatt BK, Holzschuh A, Westphal C, Clough Y, Smit I, Pawelzik E, Tscharntke T (2014) Bee pollination improves crop quality, shelf life and commercial value. Proc R Soc B 281:20132440

    PubMed  Google Scholar 

  • Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141

    CAS  Google Scholar 

  • Kukal O, Denlinger DL, Lee RE (1991) Developmental and metabolic changes induced by anoxia in diapausing and non-diapausing flesh fly pupae. J Comp Physiol B 160:683–689

    Google Scholar 

  • Lach L, Parr C, Abbott K (2010) Ant Ecology (OUP Oxford)

  • Lazić MM, Carretero MA, Crnobrnja-Isailović J, Kaliontzopoulou A (2015) Effects of environmental disturbance on phenotypic variation: an integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. Am Nat 185:44–58

    PubMed  Google Scholar 

  • Leong M, Ponisio LC, Kremen C, Thorp RW, Roderick GK (2016) Temporal dynamics influenced by global change: bee community phenology in urban, agricultural, and natural landscapes. Glob Change Biol 22:1046–1053

    Google Scholar 

  • Lessard J-P, Buddle CM (2005) The effects of urbanization on ant assemblages (Hymenoptera: Formicidae) associated with the Molson Nature Reserve. Quebec Can Entomol 137:215–225

    Google Scholar 

  • Liker A, Papp Z, Bókony V, Lendvai ÁZ (2008) Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. J Anim Ecol 77:789–795

    CAS  PubMed  Google Scholar 

  • Lowe EC, Wilder SM, Hochuli DF (2014) Urbanisation at multiple scales is associated with larger size and higher fecundity of an orb-weaving spider. PLoS ONE 9:e105480

    PubMed  PubMed Central  Google Scholar 

  • Lu P, Yu Q, Liu J, Lee X (2006) Advance of tree-flowering dates in response to urban climate change. Agric For Meteorol 138:120–131

    Google Scholar 

  • Lucas CM, Bruna EM, Nascimento CMN (2013) Seedling co-tolerance of multiple stressors in a disturbed tropical floodplain forest. Ecosphere 4:art3

    Google Scholar 

  • Luque GM, Giraud T, Courchamp F (2013) Allee effects in ants. J Anim Ecol 82:956–965

    PubMed  Google Scholar 

  • Malakar C, Ganguly A, Haldar P (2009) Influence of cadmium on growth, survival and clutch size of a common Indian short horned grasshopper, Oxya fuscovittata. Am J Toxicol Sci 1:32–36

    Google Scholar 

  • Maroni G, Wise J, Young JE, Otto E (1987) Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117:739–744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin A-J (2000) Influence of cadmium pollution on social homeostasis of red wood ants and using ants in environment bioindication. Influ Cadmium Pollut Soc Homeost Red Wood Ants Using Ants Environ Bioindic

  • McDonnell MJ, Hahs AK (2015) Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol Syst 46:261–280

    Google Scholar 

  • McDonnell MJ, Pickett STA, Groffman P, Bohlen P, Pouyat RV, Zipperer WC, Parmelee RW, Carreiro MM, Medley K (1997) Ecosystem processes along an urban-to-rural gradient. Urban Ecosyst 1:21–36

    Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176

    Google Scholar 

  • Mendes S, Colino-Rabanal VJ, Peris SJ (2011) Bird song variations along an urban gradient: The case of the European blackbird (Turdus merula). Landsc Urban Plan 99:51–57

    Google Scholar 

  • Merckx T, Souffreau C, Kaiser A, Baardsen LF, Backeljau T, Bonte D, Brans KI, Cours M, Dahirel M, Debortoli N et al (2018) Body-size shifts in aquatic and terrestrial urban communities. Nature 558:113

    CAS  PubMed  Google Scholar 

  • Miller DL, Roth MB (2009) C. Elegans are protected from lethal hypoxia by an embryonic diapause. Curr Biol 19:1233–1237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mirčić D, Janković-Tomanić M, Nenadović V, Franeta F, Lazarević J (2010) The effects of cadmium on the life history traits of Lymantria dispar L. Arch Biol Sci 62:1013–1020

    Google Scholar 

  • Modlmeier AP, Foitzik S, Scharf I (2013) Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae. Physiol Entomol 38:89–94

    Google Scholar 

  • Molet M, Péronnet R, Couette S, Canovas C, Doums C (2017) Effect of temperature and social environment on worker size in the ant Temnothorax nylanderi. J Therm Biol 67:22–29

    PubMed  Google Scholar 

  • Morgan JE, Morgan AJ (1993) Seasonal changes in the tissue-metal (Cd, Zn and Pb) concentrations in two ecophysiologically dissimilar earthworm species: pollution-monitoring implications. Environ Pollut 82:1–7

    CAS  PubMed  Google Scholar 

  • Naug D (2009) Structure and resilience of the social network in an insect colony as a function of colony size. Behav Ecol Sociobiol 63:1023–1028

    Google Scholar 

  • Partecke J, Van’t Hof T, Gwinner E (2004) Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? Proc. R Soc Lond B Biol Sci 271:1995–2001

    CAS  Google Scholar 

  • Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952

    PubMed  Google Scholar 

  • Philpott SM, Armbrecht I (2006) Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecol Entomol 31:369–377

    Google Scholar 

  • Pickett STA, Cadenasso ML, Grove JM, Nilon CH, Pouyat RV, Zipperer WC, Costanza R (2001) Urban ecological systems: linking terrestrial ecological, physical, and socioeconomic components of metropolitan areas. Annu Rev Ecol Syst 32:127–157

    Google Scholar 

  • Pillsbury FC, Miller JR (2008) Habitat and landscape characteristics underlying anuran community structure along an urban-rural gradient. Ecol Appl 18:1107–1118

    PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2016) nlme: linear and nonlinear mixed effects models, 2015. R Package Version 3:103

    Google Scholar 

  • Porter SD, Tschinkel WR (1985) Fire ant polymorphism (Hymenoptera: Formicidae): factors affecting worker size. Ann Entomol Soc Am 78:381–386

    Google Scholar 

  • Posthuma L, Van Straalen NM (1993) Heavy-metal adaptation in terrestrial invertebrates: a review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 106:11–38

    Google Scholar 

  • R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.  https://www.R-project.org/.

  • Roelofs D, Overhein L, de Boer ME, Janssens TKS, van Straalen NM (2006) Additive genetic variation of transcriptional regulation: metallothionein expression in the soil insect Orchesella cincta. Heredity 96:85

    CAS  PubMed  Google Scholar 

  • Roelofs D, Janssens TKS, Timmermans MJTN, Nota B, Mariën J, Bochdanovits Z, Ylstra B, Straalen NMV (2009) Adaptive differences in gene expression associated with heavy metal tolerance in the soil arthropod Orchesella cincta. Mol Ecol 18:3227–3239

    CAS  PubMed  Google Scholar 

  • Rubenstein DR, Abbot P (2017) Comparative Social Evolution (Cambridge University Press)

  • Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederström V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J et al (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80

    PubMed  Google Scholar 

  • Sanders D, van Veen FJF (2011) Ecosystem engineering and predation: the multi-trophic impact of two ant species. J Anim Ecol 80:569–576

    PubMed  Google Scholar 

  • Sanford MP, Manley PN, Murphy DD (2009) Effects of urban development on ant communities: implications for ecosystem services and management. Conserv Biol 23:131–141

    PubMed  Google Scholar 

  • Scales J, Hyman J, Hughes M (2011) Behavioral syndromes break down in urban song sparrow populations. Ethology 117:887–895

    Google Scholar 

  • Scharf I, Modlmeier AP, Beros S, Foitzik S (2012) Ant societies buffer individual-level effects of parasite infections. Am Nat 180:671–683

    PubMed  Google Scholar 

  • Schultz TR (2000) In search of ant ancestors. Proc Natl Acad Sci U S A 97:14028–14029

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seto KC, Güneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci 109:16083–16088

    CAS  PubMed  Google Scholar 

  • Slabbekoorn H, den Boer-Visser A (2006) Cities Change the Songs of Birds. Curr Biol 16:2326–2331

    CAS  PubMed  Google Scholar 

  • Starý P, Kubizňáková J (1987) Content and transfer of heavy metal air pollutants in populations of spp. wood ants (Hym., Formicidae). J Appl Entomol 104:1–10

    Google Scholar 

  • Stroiński A (1999) Some physiological and biochemical aspects of plant resistance to cadmium effect. I Antioxidative system Acta Physiol Plant 21:175–188

    Google Scholar 

  • Tlili A, Maréchal M, Bérard A, Volat B, Montuelle B (2011) Enhanced co-tolerance and co-sensitivity from long-term metal exposures of heterotrophic and autotrophic components of fluvial biofilms. Sci Total Environ 409:4335–4343

    CAS  PubMed  Google Scholar 

  • van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ (2016) The industrial melanism mutation in British peppered moths is a transposable element. Nature 534:102–105

    PubMed  Google Scholar 

  • Vesela S, Vijverberg J (2007) Effect of body size on toxicity of zinc in neonates of four differently sized daphnia species. Aquat Ecol 41:67–73

    CAS  Google Scholar 

  • Weller B, Ganzhorn JU (2004) Carabid beetle community composition, body size, and fluctuating asymmetry along an urban-rural gradient. Basic Appl Ecol 5:193–201

    Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R (Springer Science & Business Media)

Download references

Acknowledgements

We thank the Agence Nationale de la Recherche (ANR Grant number: ANTEVOANR-12-JSV7-0003-01) and the Institut de la Transition Environnementale de Sorbonne Université (ITE-SU) for their fundings. We would like to thank David Siaussat for his advices with the LC50 choice, Marine Güell and Clément Car for their help in the maintenance of colonies and the collection of lab workers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Jacquier.

Electronic supplementary material

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jacquier, L., Doums, C., Four-Chaboussant, A. et al. Urban colonies are more resistant to a trace metal than their forest counterparts in the ant Temnothorax nylanderi. Urban Ecosyst 24, 561–570 (2021). https://doi.org/10.1007/s11252-020-01060-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11252-020-01060-9

Keywords

Navigation