Larvae promote a decline in the harvesting of myrmecochorous seeds by Myrmica rubra ants

  • A. Bologna
  • C. DetrainEmail author
Research Article


Non-granivorous ant species that contribute to seed dispersal (myrmecochory sensu stricto) are assumed to benefit from the larval consumption of elaiosomes, the lipid-rich appendages of myrmecochorous seeds. It is, however, questionable whether this ant–plant interaction is truly mutualistic, since some ant partners do not show a clear-cut fitness gain and may cease the harvesting of myrmecochorous seeds over time. In particular, the role of ant larvae as potential consumers of seed elaiosomes is not yet fully understood. In this study, we investigated how the number of larvae influences the foraging responses of the red ant Myrmica rubra to Viola odorata myrmecochorous seeds and to Drosophila melanogaster prey. Ant workers retrieved less elaiosome-bearing seeds than prey and the harvesting of seeds remained low, even in the presence of larvae. Furthermore, while the ant colonies continued to collect prey over successive foraging events, the retrieval of myrmecochorous seeds decreased, most particularly in colonies containing a large number of larvae. Brood exposure to diaspores also declined, with very few larvae coming into contact with seeds. Our results suggest that the role of larvae as elaiosome consumers should be reconsidered and that larvae may provide workers with cues about the poor palatability of V. odorata diaspores, thereby altering the stability of this ant–plant interaction.


Common red ant Sweet violet Ant–plant interactions Myrmecochory Foraging Brood number 



This work was supported by a Belgian PhD Grant from the F.R.I.A. (Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture) attributed to A. Bologna. Dr Claire Detrain is Research Director from the Belgian National Fund for Scientific Research (F.N.R.S).


  1. Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge. CrossRefGoogle Scholar
  2. Berg RY (1975) Myrmecochorous plants in Australia and their dispersal by ants. Aust J Bot 23:475. CrossRefGoogle Scholar
  3. Bologna A, Detrain C (2015) Steep decline and cessation in seed dispersal by Myrmica rubra ants. PLoS One 10:e0139365. CrossRefGoogle Scholar
  4. Bono JM, Heithaus ER (2002) Sex ratios and the distribution of elaiosomes in colonies of the ant, Aphaenogaster rudis. Insectes Soc 49:320–325. CrossRefGoogle Scholar
  5. Brew CR, Dowd DJO, Rae ID, Url S (1989) Seed dispersal by ants: behaviour-releasing compounds in elaiosomes. Oecologia 80:490–497. CrossRefGoogle Scholar
  6. Bulow-Olsen A (1984) Diplochory in Viola: a possible relation between seed dispersal and soil seed bank. Am Midl Nat 112:251–260CrossRefGoogle Scholar
  7. Cammaerts M (1977) Recrutement d’ouvrières vers une source d’eau pure ou sucrée chez la fourmi Myrmica ruba L. Biol Behav 2:287–308Google Scholar
  8. Cassill D (2003) Rules of supply and demand regulate recruitment to food in an ant society. Behav Ecol Sociobiol 54:441–450. CrossRefGoogle Scholar
  9. Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, Solenopsis invicta. Anim Behav 50:801–813. CrossRefGoogle Scholar
  10. Cassill DL, Tschinkel WR (1999) Information flow during social feeding in ant societies. In: Detrain et al (eds) Information processing in social insects. Birkhauser, Basel, pp 69–81. CrossRefGoogle Scholar
  11. Cassill DL, Butler J, Vinson SB, Wheeler DE (2005) Cooperation during prey digestion between workers and larvae in the ant, Pheidole spadonia. Insectes Soc 52:339–343. CrossRefGoogle Scholar
  12. Caut S, Jowers MJ, Cerda X, Boulay RR (2013) Questioning the mutual benefits of myrmecochory: a stable isotope-based experimental approach. Ecol Entomol 38:390–399. CrossRefGoogle Scholar
  13. Chen G, Huang S-Z, Chen S-C et al (2016) Chemical composition of diaspores of the myrmecochorous plant Stemona tuberosa Lour. Biochem Syst Ecol 64:31–37. CrossRefGoogle Scholar
  14. Culver DC, Beattie AJ (1978) Myrmecochory in Viola: dynamics of seed–ant interactions in some west Virginia species. J Ecol 66:53–72CrossRefGoogle Scholar
  15. Culver DC, Beattie AJ (1980) The fate of Viola seeds dispersed by ants. Am J Bot 67:710–714. CrossRefGoogle Scholar
  16. Detrain C, Bologna A (2019) Impact of seed abundance on seed processing and dispersal by the red ant Myrmica rubra. Ecol Entomol 44:380–388. CrossRefGoogle Scholar
  17. Detrain C, Tasse O (2000) Seed drops and caches by the harvester ant Messor barbarus: do they contribute to seed dispersal in Mediterranean grasslands? Naturwissenschaften 87:373–376. CrossRefGoogle Scholar
  18. Dostál P (2005) Effect of three mound-building ant species on the formation of soil seed bank in mountain grassland. Flora 200:148–158. CrossRefGoogle Scholar
  19. Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744. CrossRefGoogle Scholar
  20. Fischer RC, Ölzant SM, Wanek W, Mayer V (2005) The fate of Corydalis cava elaiosomes within an ant colony of Myrmica rubra: elaiosomes are preferentially fed to larvae. Insectes Soc 52:55–62. CrossRefGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. Fokuhl G, Heinze J, Poschlod P (2007) Colony growth in Myrmica rubra with supplementation of myrmecochorous seeds. Ecol Res 22:845–847. CrossRefGoogle Scholar
  23. Fokuhl G, Heinze J, Poschlod P (2012) Myrmecochory by small ants—beneficial effects through elaiosome nutrition and seed dispersal. Acta Oecol 38:71–76. CrossRefGoogle Scholar
  24. Gammans N, Bullock JM, Schönrogge K, James M (2005) Ant benefit in a seed dispersal mutualism. Oecologia 146:43–49. CrossRefGoogle Scholar
  25. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oecologia 3:481–492. Google Scholar
  26. Gorb E, Gorb S (2000) Effects of seed aggregation on the removal rates of elaiosome-bearing Chelidonium majus and Viola odorata seeds carried by Formica polyctena ants. Ecol Res 15:187–192. CrossRefGoogle Scholar
  27. Gove AD, Majer JD, Dunn RR (2007) A keystone ant species promotes seed dispersal in a “diffuse” mutualism. Oecologia 153:687–697. CrossRefGoogle Scholar
  28. Handel SN (1978) The competitive relationship of three wood land sedges and its bearing on the evolution of ant dispersal of Carex pedunculata. Evolution 32(151):163. Google Scholar
  29. Heithaus ER (1981) Seed predation by rodents on three ant-dispersed plants. Ecology 62:136–145. CrossRefGoogle Scholar
  30. Heithaus ER, Heithaus P, Liu SY (2005) Satiation in collection of myrmecochorous diaspores by colonies of Aphaenogaster rudis (Formicidae: myrmicinae) in Central Ohio, USA. J Insect Behav 18:827–846. CrossRefGoogle Scholar
  31. Horvitz CC (1981) Analysis of how ant behaviors affect germination in a tropical myrmecochore Calathea microcephala (P.&E.) Koernicke (Marantaceae): microsite selection and aril removal by neotropical ants, Odontomachus, Pachycondyla, and Solenopsis (Formicidae). Oecologia 20:47–52. CrossRefGoogle Scholar
  32. Horvitz CC, Beattie AJ (1980) Ant dispersal of Calathea (Marantaceae) seeds by carnivorous ponerines (Formicidae) in a tropical rain forest. Am J Bot 67:321–326. CrossRefGoogle Scholar
  33. Hughes L, Westoby M (1992) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299. CrossRefGoogle Scholar
  34. Hughes L, Westoby M, Jurado E (1994) Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition. Funct Ecol 8:358–365CrossRefGoogle Scholar
  35. Lambinon J, Verloove F (2012) Nouvelle flore de la Belgique, du G.-D. de Luxembourg, du nord de la France et des régions voisines. 6th Ed. Jardin Botanique- Plantentuin, MeiseGoogle Scholar
  36. Lanza J, Schmitt M, Awad A (1992) Comparative chemistry of elaiosomes of three species of Trillium. J Chem Ecol 18:209–221. CrossRefGoogle Scholar
  37. Leal LC, Neto MCL, de Oliveira AFM et al (2014) Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae in Brazilian Caatinga. Oecologia 174:493–500. CrossRefGoogle Scholar
  38. Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RB (2009) Ants sow the seeds of global diversification in flowering plants. Public Libr Sci One 4:e5480Google Scholar
  39. Marshall DL, Beattie J, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant-seed interaction. J Chem Ecol 5:335–344. CrossRefGoogle Scholar
  40. Marussich W (2006) Testing myrmecochory from the ant’s perspective: the effects of Datura wrightii and D. discolor on queen survival and brood production in Pogonomyrmex californicus. Insectes Soc 53:403–411. CrossRefGoogle Scholar
  41. Morales M, Heithaus ER (1998) Food from seed-dispersal mutualism shifts sex ratios in colonies of the ant Aphaenogaster rudis. Ecology 79:734–739CrossRefGoogle Scholar
  42. Ohkawara K (2005) Effect of timing of elaiosome removal on seed germination in the ant-dispersed plant, Erythronium japonicum (Liliaceae). Plant Species Biol 20:145–148. CrossRefGoogle Scholar
  43. Pfeiffer M, Huttenlocher H, Ayasse M (2010) Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants. Funct Ecol 24:545–555. CrossRefGoogle Scholar
  44. Reifenrath K, Becker C, Poethke HJ (2012) Diaspore trait preferences of dispersing ants. J Chem Ecol 38:1093–1104. CrossRefGoogle Scholar
  45. Rico-gray V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, ChicagoGoogle Scholar
  46. Servigne P, Detrain C (2008) Ant-seed interactions: combined effects of ant and plant species on seed removal patterns. Insectes Soc 55:220–230. CrossRefGoogle Scholar
  47. Servigne P, Detrain C (2010) Opening myrmecochory’s black box: what happens inside the ant nest? Ecol Res 25:663–672. CrossRefGoogle Scholar
  48. Turner KM, Frederickson ME (2013) Signals can trump rewards in attracting seed-dispersing ants. PLoS One 8:e71871. CrossRefGoogle Scholar
  49. Warren RJ II, Giladi I (2014) Ant-mediated seed dispersal: a few ant species (Hymenoptera:Formicidae) benefit many plants. Myrmecol News 20:129–140Google Scholar
  50. Warren RJ, Elliott K, Giladi I, King JR, Bradford MA (2019) Field experiments show contradictory short-and long-term myrmecochorous plant impacts on seed-dispersing ants. Ecol Entomol 44:30–39. CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2019

Authors and Affiliations

  1. 1.Service d’Ecologie Sociale, CP 231Université Libre de Bruxelles (ULB)BrusselsBelgium

Personalised recommendations