Skip to main content

Advertisement

Log in

Cheaters and removalists: the influence of soil disturbance on ant–seed interactions in roadside vegetation

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Myrmecochory is an important mutualistic interaction, where ants provide seed dispersal services for many plant species. We examined the influence of soil disturbances associated with roadworks activity on ant–seed interactions in roadside environments in south-eastern Australia. In the study landscape, minor rural road reserves often provide critical habitat for endangered species and woodland ecosystems. We conducted seed-depot experiments to quantify the extent of ant–seed removal, and identified the contribution of different ant species to seed removal and elaiosome consumption (cheating) interactions, in disturbed and non-disturbed roadside zones. Twenty-six ant species were recorded interacting with seeds; however, only a few species were responsible for dispersing most seeds. We found soil disturbance and roadside width influenced observed ant–seed interactions, which was largely explained by individual species habitat and behavioural traits. Iridomyrmex purpureus removed a higher proportion of seeds in soil disturbed zones, while Rhytidoponera metallica carried out more seed removals in narrow roadsides. R. metallica and Melophorus bruneus typically carried out seed removals (only), while Monomorium and Pheidole spp. almost exclusively carried out cheating behaviours. These results highlight the complex nature of ant–plant interactions is association with novel soil disturbance regimes, where ants perform a critical seed dispersal service for myrmecochorous roadside vegetation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen AN (1992) Regulation of “momentary” diversity by dominant species in exceptionally rich ant communities of the Australian seasonal tropics. Am Nat 140:401–420

    CAS  PubMed  Google Scholar 

  • Andersen AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. J Biogeogr 22:15–29

    Google Scholar 

  • Andersen AN (2019) Responses of ant communities to disturbance: five principles for understanding the disturbance dynamics of a globally dominant faunal group. J Anim Ecol 88:350–362

    PubMed  Google Scholar 

  • Andersen AN, Morrison SC (1998) Myrmecochory in Australia’s seasonal tropics: effects of disturbance on distance dispersal. Austral Ecol 23:483–491

    Google Scholar 

  • Andersen AN, Azcarate FM, Cowie ID (2000) Seed selection by an exceptionally rich community of harvester ants in the Australian seasonal tropics. J Anim Ecol 69:975–984

    Google Scholar 

  • Andrew NR, Hart RA, Jung MP, Hemmings Z, Terblanche JS (2013) Can temperate insects take the heat? A case study of the physiological and behavioural responses in a common ant, Iridomyrmex purpureus (Formicidae), with potential climate change. J Insect Physiol 59:870–880

    CAS  PubMed  Google Scholar 

  • Aranda-Rickert A, Fracchia S (2011) Pogonomyrmex cunicularius as the keystone disperser of elaiosome-bearing Jatropha excisa seeds in semi-arid Argentina. Entomol Exp Appl 139:91–102

    Google Scholar 

  • Arnan X, Molowny-Horas R, Rodrigo A, Retana J (2012) Uncoupling the effects of seed predation and seed dispersal by granivorous ants on plant population dynamics. PLoS ONE 7:e42869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnan X, Cerdá X, Rodrigo A, Retana J (2013) Response of ant functional composition to fire. Ecography 36:1182–1192

    Google Scholar 

  • Auld TD, Denham AJ (1999) The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae). Plant Ecol 144:201–213

    Google Scholar 

  • Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge

    Google Scholar 

  • Beattie AJ, Hughes L (2002) Ant–plant interactions. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 211–235

    Google Scholar 

  • Beaumont KP, Mackay DA, Whalen MA (2011) Interactions between ants and seeds of two myrmecochorous plant species in recently burnt and long-unburnt forest sites. Austral Ecol 36:767–778

    Google Scholar 

  • Beaumont KP, Mackay DA, Whalen MA (2012) The effects of prescribed burning on epigaeic ant communities in eucalypt forest of South Australia. For Ecol Manag 271:147–157

    Google Scholar 

  • Beaumont KP, Mackay DA, Whalen MA (2013) Multiphase myrmecochory: the roles of different ant species and effects of fire. Oecologia 172:791–803

    PubMed  Google Scholar 

  • Bennett AF (1991) Roads, roadsides and wildlife conservation: a review. In: Saunders DA, Hobbs RJ (eds) Nature conservation 2: the role of corridors. Surrey Beatty, Chipping Norton, pp 99–118

    Google Scholar 

  • Berg R (1975) Myrmecochorous plants in Australia and their dispersal by ants. Aust J Bot 23:475–508

    Google Scholar 

  • Bognounou F, Savadogo P, Thiombiano A, Tigabu M, Boussim IJ, Oden PC, Guinko S (2009) Impact of disturbance from roadworks on Pteleopsis suberosa regeneration in roadside environments in Burkina Faso, West Africa. J For Res 20:355–361

    Google Scholar 

  • Brew CR, O'Dowd DJ, Rae ID (1989) Seed dispersal by ants: behaviour-releasing compounds in elaiosomes. Oecologia 80:490–497

    PubMed  Google Scholar 

  • Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287

    Google Scholar 

  • Buckley RP (1982) Ant–plant interactions in Australia. Springer, The Hague

    Google Scholar 

  • Bull L (1997) Lockhart shire roadside vegetation survey and recommendations. Lockhart Shire Council, Lockhart

    Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    CAS  PubMed  Google Scholar 

  • Christianini A, Oliveira P (2013) Edge effects decrease ant-derived benefits to seedlings in a neotropical savanna. Arthropod-Plant Interact 7:191–199

    Google Scholar 

  • Crist TO (2009) Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: a review. Myrmecol News 12:3–13

    Google Scholar 

  • Cuautle M, Rico-Gray V, Diaz-Castelazo C (2005) Effects of ant behaviour and presence of extrafloral nectaries on seed dispersal of the Neotropical myrmecochore Turnera ulmifolia L. (Turneraceae). Biol J Linn Soc 86:67–77

    Google Scholar 

  • Espadaler XC, Gomez C, Suiter D (1995) Seed-robbing between ant species intervenes in the myrmecochory of Euphorbia characias (Euphorbiaceae). Psyche 102:19–25

    Google Scholar 

  • Fischer RC, Richter A, Hadacek F, Mayer V (2008) Chemical differences between seeds and elaiosomes indicate an adaptation to nutritional needs of ants. Oecologia 155:539–547

    PubMed  Google Scholar 

  • Garrido JL, Rey PJ, Cerdá X, Herrera CM (2002) Geographical variation in diaspore traits of an ant-dispersed plant (Helleborus foetidus): Are ant community composition and diaspore traits correlated? J Ecol 90:446–455

    Google Scholar 

  • Gibb H (2005) The effect of a dominant ant, Iridomyrmex purpureus, on resource use by ant assemblages depends on microhabitat and resource type. Austral Ecol 30:856–867

    Google Scholar 

  • Gibb H, Hochuli DF (2003) Colonisation by a dominant ant facilitated by anthropogenic disturbance: effects on ant assemblage composition, biomass and resource use. Oikos 103:469–478

    Google Scholar 

  • Gibb H, Parr CL (2010) How does habitat complexity affect ant foraging success? A test using functional measures on three continents. Oecologia 164:1061–1073

    CAS  PubMed  Google Scholar 

  • Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492

    Google Scholar 

  • Gillison AN (1994) Woodlands. In: Groves RH (ed) Australian vegetation, 2nd edn. Cambridge University Press, Melbourne, pp 227–255

    Google Scholar 

  • Gove AD, Majer JD, Dunn RR (2007) A keystone ant species promotes seed dispersal in a diffuse mutualism. Oecologia 153:687–697

    PubMed  Google Scholar 

  • Greaves T (1971) The distribution of the tree forms of the meat ant Iridomymrex purpureus (Hymenoptera: Formicidae) in Australia. Aust J Entomol 10:15–21

    Google Scholar 

  • Greenslade PJM (1976) Meat ant Iridomyrmex purpureus (Hymenoptera: Formicidae) as a dominant member of ant communities. Aust J Entomol 15:237–240

    Google Scholar 

  • Harris RJ, Standish RJ (2008) Ant dispersal and predation affects the availability of seeds for old-field recolonisation in Western Australia. J R Soc West Aust 91:301–311

    Google Scholar 

  • Heithaus ER, Humes M (2003) Variation in communities of seed-dispersing ants in habitats with different disturbance in Knox County, Ohio. Ohio J Sci 103:89–97

    Google Scholar 

  • Hoffmann BD, Andersen AN (2003) Responses of ants to disturbance in Australia, with particular reference to functional groups. Austral Ecol 28:444–464

    Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228

    Google Scholar 

  • Hughes L, Westoby M (1990) Removal rates of seeds adapted for dispersal by ants. Ecology 71:138–148

    Google Scholar 

  • Hughes L, Westoby M (1992) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299

    Google Scholar 

  • Jones EI, Afkhami ME, Akçay E et al (2015) Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism. Ecol Lett 18:1270–1284

    PubMed  Google Scholar 

  • Kaur H, Torma A, Gallé-Szpisjak N, Šeat J, Lőrinczi G, Módra G, Gallé R (2019) Road verges are important secondary habitats for grassland arthropods. J Insect Cons 23:899–907

    Google Scholar 

  • Leal LC, Andersen AN, Leal IR (2013) Anthropogenic disturbance reduces seed-dispersal services for myrmecochorous plants in the Brazilian Caatinga. Oecologia 174:173–181

    PubMed  Google Scholar 

  • Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2010) Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: a global survey. Perspect Plant Ecol Evol Syst 12:43–55

    Google Scholar 

  • Lubertazzi D, Aliberti Lubertazzi MA, McCoy N, Gove AD, Majer JD, Dunn RR (2010) The ecology of a keystone seed disperser, the ant Rhytidoponera violacea. J Insect Sci 10:1–15

    Google Scholar 

  • Majer JD (1982) Ant–plant interactions in the Darling Botanical District of Western Australia. In: Buckley R (ed) Ant–plant interactions in Australia, Dr W. Junk Publishers, Dordrecht, pp 45–61

    Google Scholar 

  • Majer JD, Gove AD, Sochacki S, Searle P, Portlock C (2011) A comparison of the autecology of two seed-taking ant genera, Rhytidoponera and Melophorus. Insect Soc 58:115–125

    Google Scholar 

  • Major RE, Smith D, Cassis G, Gray M, Colgan DJ (1999) Are roadside strips important reservoirs of invertebrate diversity? A comparison of the ant and beetle faunas of roadside strips and large remnant woodlands. Aust J Zool 47:611–624

    Google Scholar 

  • Manzaneda AJ, Rey PJ (2009) Assessing ecological specialization of an ant–seed dispersal mutualism through a wide geographic range. Ecol 90:3009–3022

    Google Scholar 

  • Manzaneda AJ, Rey PJ, Boulay R (2007) Geographic and temporal variation in the ant-seed dispersal assemblage of the perennial herb Helleborus foetidus L. (Ranunculaceae). Biol J Linn Soc 92:135–150

    Google Scholar 

  • Mitchell CE, Turner MG, Pearson SM (2002) Effects of historical land use and forest patch size on myrmecochores and ant communities. Ecol Appl 12:1364–1377

    Google Scholar 

  • Morton SR (1985) Granivory in arid regions: comparison of Australia with North and South America. Ecol 66:1859–1866

    Google Scholar 

  • Ness JH, Morin DF (2008) Forest edges and landscape history shape interactions between plants, seed-dispersing ants and seed predators. Biol Cons 141:838–847

    Google Scholar 

  • Ness JH, Morin DF, Giladi I (2009) Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: Are Aphaenogaster ants keystone mutualists? Oikos 118:1793–1804

    Google Scholar 

  • Palfi Z, Spooner PG, Robinson W (2017a) Soil disturbance effects on the composition of seed-dispersing ants in roadside environments. Oecologia 183:493–503

    PubMed  Google Scholar 

  • Palfi Z, Spooner PG, Robinson W (2017b) Seed dispersal distances by ants increase in response to anthropogenic disturbances in Australian roadside environments. Front Ecol Evol 132:1–9

    Google Scholar 

  • Parr CL, Andersen AN, Chastagnol C, Duffaud C (2007) Savanna fires increase rates and distances of seed dispersal by ants. Oecologia 151:33–41

    CAS  PubMed  Google Scholar 

  • Pascov CM, Nevill PG, Elliott CP, Majer JD, Anthony JM, Krauss SL (2015) The critical role of ants in the extensive dispersal of Acacia seeds revealed by genetic parentage assignment. Oecologia 179:1123–1134

    PubMed  Google Scholar 

  • Planqué R, Van Den Berg JB, Franks NR (2010) Recruitment strategies and colony size in ants. PLoS ONE 5(8):e11664

    PubMed  PubMed Central  Google Scholar 

  • Pudlo RJ, Beattie AJ, Culver DC (1980) Population consequences of changes in an ant-seed mutualism in Sanguinaria canadensis. Oecologia 46:32–37

    PubMed  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, Chicago

    Google Scholar 

  • SAS (2013) SAS/STAT® 13.1 user’s guide. SAS Institute Inc., Cary, NC

    Google Scholar 

  • SAS (2015) SAS studio version 9.04.01. SAS Institute Inc., Cary, NC

    Google Scholar 

  • Shattuck SO (1999) Australian ants: their biology and identification. CSIRO Publishing, Collingwood

    Google Scholar 

  • Spooner PG (2005) On squatters, settlers and early surveyors: historical development of country road reserves in southern New South Wales. Aust Geogr 36:55–73

    Google Scholar 

  • Spooner PG (2015) Minor rural road networks: values, challenges, and opportunities for biodiversity conservation. Nat Conserv 11:129–142

    Google Scholar 

  • Spooner PG, Lunt ID (2004) The influence of land-use history on roadside conservation values in an Australian agricultural landscape. Aust J Bot 52:445–458

    Google Scholar 

  • Spooner PG, Lunt ID, Briggs SV, Freudenberger D (2004) Effects of soil disturbance from roadworks on roadside shrubs in a fragmented agricultural landscape. Biol Cons 117:393–406

    Google Scholar 

  • Suárez-Esteban A, Delibes M, Fedriani JM (2013) Barriers or corridors? The overlooked role of unpaved roads in endozoochorous seed dispersal. J Appl Ecol 50:767–774

    Google Scholar 

  • Tame T (1992) Acacias of Southeast Australia. Kangaroo Press, Kenthurst

    Google Scholar 

  • Vieira-Neto EH, Vasconcelos HL, Bruna EM (2016) Roads increase population growth rates of a native leaf-cutter ant in Neotropical savannahs. J Appl Ecol 53:983–992

    Google Scholar 

  • Vonshak M, Gordon DM (2015) Intermediate disturbance promotes invasive ant abundance. Biol Cons 186:359–367

    Google Scholar 

  • Warren RJ, Giladi I (2014) Ant-mediated seed dispersal: a few ant species (Hymenoptera: Formicidae) benefit many plants. Myrmecol News 20:129–140

    Google Scholar 

  • Whitney KD (2002) Dispersal for distance? Acacia ligulata seeds and meat ants Iridomyrmex viridiaeneus. Austral Ecol 27:589–595

    Google Scholar 

  • Yates CJ, Hobbs RJ (1997) Temperate eucalypt woodlands: a review of their status, processes threatening their persistence and techniques for restoration. Aust J Bot 45:949–973

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall International, Sydney

    Google Scholar 

  • Zelikova TJ, Breed MD (2008) Effects of habitat disturbance on ant community composition and seed dispersal by ants in a tropical dry forest in Costa Rica. J Trop Ecol 24:309–316

    Google Scholar 

Download references

Acknowledgements

A postgraduate scholarship from Charles Sturt University was provided to ZP to complete her doctoral research, of which this work is a component. We are grateful to Levente Palfi for field work assistance and thank Alan N. Andersen for assistance with the identification of ant species. We would also like to thank two anonymous reviewers whose comments have greatly improved the quality of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. G. Spooner.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This study was carried out in accordance with Australian Code of Practice for the care and use of animals for scientific purposes and Charles Sturt University Animal Care and Ethics Committee policy. The study did not involve endangered or protected species and we did not collect ants in protected areas.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Palfi, Z., Robinson, W. & Spooner, P.G. Cheaters and removalists: the influence of soil disturbance on ant–seed interactions in roadside vegetation. Insect. Soc. 67, 429–438 (2020). https://doi.org/10.1007/s00040-020-00778-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-020-00778-1

Keywords

Navigation