Advertisement

Oecologia

, Volume 172, Issue 3, pp 791–803 | Cite as

Multiphase myrmecochory: the roles of different ant species and effects of fire

  • Kieren P. BeaumontEmail author
  • Duncan A. Mackay
  • Molly A. Whalen
Plant-animal interactions - Original research

Abstract

Seed dispersal by ants (myrmecochory) can be influenced by changes to ant assemblages resulting from habitat disturbance as well as by differences in disperser behaviour. We investigated the effect of habitat disturbance by fire on the dispersal of seeds of a myrmecochorous shrub, Pultenaea daphnoides. We also investigated the consequence of the seed relocation behaviours of two common dispersers (Pheidole sp. A and Rhytidoponera metallica) for the redispersal of seeds. Pheidole sp. A colonies did not relocate seeds outside their nests. In contrast, R. metallica colonies relocated 43.6 % of seeds fed to them, of which 96.9 % had residual elaiosome that remained attached. On average, R. metallica relocated seeds 78.9 and 60.7 cm from the nest entrances in burned and unburned habitat, respectively. Seeds were removed faster in burned than in unburned habitat, and seeds previously relocated by R. metallica were removed at similar rates to seeds with intact elaiosomes, but faster than seeds with detached elaiosomes. Dispersal distances were not significantly different between burned (51.3 cm) and unburned (70.9 cm) habitat or between seeds with different elaiosome conditions. Differences between habitat types in the frequency of seed removal, the shape of the seed dispersal curve, and the relative contribution of R. metallica and Pheidole sp. A to seed dispersal were largely due to the effect of recent fire on the abundance of Pheidole sp. A. Across habitat types, the number of seeds removed from depots and during dispersal trials most strongly related to the combined abundances of R. metallica and Pheidole. Our findings show that myrmecochory can involve more than one dispersal phase and that fire indirectly influences myrmecochory by altering the abundances of seed-dispersing ants.

Keywords

Ant Disturbance Dispersal distance Prescribed burn Rhytidoponera 

Notes

Acknowledgments

This research was funded by the Wildlife Conservation Fund, the Native Vegetation Council of South Australia, Mark Mitchell Research Foundation and the Holsworth Wildlife Research Endowment. We thank M. Hendersen (Department for Environment, Water and Natural Resources) for information regarding fire histories, B. Heterick for identifying the ants and Cleland Conservation Park staff for access to field sites. Finally, we thank three anonymous reviewers whose comments greatly improved this manuscript. The experiments comply with the current laws of Australia.

Supplementary material

Supplementary material 1 (MPG 21246 kb)

442_2012_2534_MOESM2_ESM.doc (76 kb)
Supplementary material 2 (DOC 76 kb)

References

  1. Andersen AN (1988a) Dispersal distance as a benefit of myrmecochory. Oecologia 75:507–511. doi: 10.1007/BF00776412 CrossRefGoogle Scholar
  2. Andersen AN (1988b) Immediate and longer-term effects of fire on seed predation by ants in sclerophyllous vegetation in south-eastern Australia. Aust J Ecol 13:285–293. doi: 10.1111/j.1442-9993.1988.tb00976.x CrossRefGoogle Scholar
  3. Andersen AN (1991) Responses of ground-foraging ant communities to three experimental fire regimes in a savanna forest of tropical Australia. Biotropica 23:575–585. doi: 10.2307/2388395 CrossRefGoogle Scholar
  4. Andersen AN, Morrison SC (1998) Myrmecochory in Australia’s seasonal tropics: effects of disturbance on distance dispersal. Aust J Ecol 23:483–491. doi: 10.1111/j.1442-9993.1998.tb00756.x CrossRefGoogle Scholar
  5. 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. doi: 10.1111/j.1570-7458.2011.01111.x CrossRefGoogle Scholar
  6. Arnan X, Rodrigo A, Molowny-Horas R, Retana J (2010) Ant-mediated expansion of an obligate seeder species during the first years after fire. Plant Biol 12:842–852. doi: 10.1111/j.1438-8677.2009.00294.x PubMedCrossRefGoogle Scholar
  7. Auld TD (1986) Population dynamics of the shrub Acacia suaveolens (Sm.) Willd.: dispersal and dynamics of the soil seed-bank. Aust J Ecol 11:235–354. doi: 10.1111/j.1442-9993.1986.tb01395.x CrossRefGoogle Scholar
  8. 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. doi: 10.1023/A:1009817132378 CrossRefGoogle Scholar
  9. Auld TD, O’Connell MA (1991) Predicting patterns of post-fire germination in 35 eastern Australian Fabaceae. Aust J Ecol 16:53–70. doi: 10.1111/j.1442-9993.1991.tb01481.x CrossRefGoogle Scholar
  10. Bas JM, Oliveras J, Gomez C (2009) Myrmecochory and short-term seed fate in Rhamnus alaternus: ant species and seed characteristics. Acta Oecol 35:380–384. doi: 10.1016/j.actao.2009.02.003 CrossRefGoogle Scholar
  11. Bates D, Maechler M (2010) lme4: linear mixed-effects models using S4 classes. In: R package version 0999375-33. http://CRANR-projectogr/package=lme4
  12. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, CambridgeGoogle Scholar
  13. Beattie AJ, Culver DC (1983) The nest chemistry of two seed-dispersing ant species. Oecologia 56:99–103. doi: 10.1007/BF00378223 CrossRefGoogle Scholar
  14. Beaumont KP, Mackay DA, Whalen MA (2009) Combining distances of ballistic and myrmecochorous seed dispersal in Adriana quadripartita (Euphorbiaceae). Acta Oecol 35:429–436. doi: 10.1016/j.actao.2009.01.005 CrossRefGoogle Scholar
  15. Beaumont KP, Mackay DA, Whalen MA (2011) Interactions between ants and seed of two myrmecochorous plant species in recently-burnt and long unburnt forest sites. Aust Ecol 36:767–778. doi: 10.1111/j.1442-9993.2010.02215.x CrossRefGoogle Scholar
  16. 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. doi: 10.1016/j.foreco.2012.02.007 CrossRefGoogle Scholar
  17. Berg RY (1975) Myrmecochorous plants in Australia and their dispersal by ants. Aust J Bot 23:475–508. doi: 10.1071/BT9750475 CrossRefGoogle Scholar
  18. Bond WJ, Slingsby P (1984) Collapse of an ant-plant mutualism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 65:1031–1037. doi: 10.2307/1938311 CrossRefGoogle Scholar
  19. Boyd RS (2001) Ecological benefits of myrmecochory for the endangered chaparral shrub Fremontodendron decumbens (Sterculiaceae). Am J Bot 88:234–241. doi: 10.2307/2657014 PubMedCrossRefGoogle Scholar
  20. Bradstock RA, Auld TD (1995) Soil temperatures during experimental bushfires in relation to fire intensity: consequences for legume germination and fire management in south-eastern Australia. J Appl Ecol 32:76–84. doi: 10.2307/2404417 CrossRefGoogle Scholar
  21. Bresinsky A (1963) Bau, entwicklungsgeschichte und inhaltsstoffe der elaiosomen. Bibl Bot 126:1–54Google Scholar
  22. Brew CR, O’Dowd DJ, Rae ID (1989) Seed dispersal by ants—behavior-releasing compounds in elaiosomes. Oecologia 80:490–497. doi: 10.1007/BF00380071 CrossRefGoogle Scholar
  23. Canner JE, Spence M (2011) A new technique using metal tags to track small seeds over short distances. Ecol Res 26:233–236. doi: 10.1007/s11284-010-0761-8 CrossRefGoogle Scholar
  24. Canner JE, Dunn RR, Giladi I, Gross K (2012) Redispersal of seeds by a keystone ant augments the spread of common wildflowers. Acta Oecol 40:31–39. doi: 10.1016/j.actao.2012.02.004 CrossRefGoogle Scholar
  25. Christian CE, Stanton ML (2004) Cryptic consequences of a dispersal mutualism: seed burial, elaiosome removal, and seed-bank dynamics. Ecology 85:1101–1110. doi: 10.1890/03-0059 CrossRefGoogle Scholar
  26. Davidson DW, Morton SR (1981) Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone. Oecologia 50:357–366. doi: 10.1007/BF00344976 CrossRefGoogle Scholar
  27. Drake WE (1981) Ant–seed interaction in dry sclerophyll forest on north Stradbroke Island, Queensland. Aust J Bot 29:293–309. doi: 10.1071/BT9810293 CrossRefGoogle Scholar
  28. Gammans N, Bullock JM, Schonrogge K (2005) Ant benefits in a seed dispersal mutualism. Oecologia 146:43–49. doi: 10.1007/s00442-005-0154-9 PubMedCrossRefGoogle Scholar
  29. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492. doi: 10.1111/j.0030-1299.2006.14258.x CrossRefGoogle Scholar
  30. Gimeno-Garcia E, Andreu V, Rubio JL (2004) Spatial patterns of soil temperatures during experimental fires. Geoderma 118:17–38. doi: 10.1016/S0016-7061(03)00167-8 CrossRefGoogle Scholar
  31. Gomez C, Espadaler X (1998a) Seed dispersal curve of a Mediterranean myrmecochore: influence of ant size and the distance to nests. Ecol Res 13:347–354. doi: 10.1046/j.1440-1703.1998.00274.x CrossRefGoogle Scholar
  32. Gomez C, Espadaler X (1998b) Aphaenogaster senilis Mayr (Hymenoptera, Formicidae): a possible parasite in the myrmecochory of Euphorbia characias (Euphorbiaceae). Sociobiology 32:441–450Google Scholar
  33. Gomez C, Espadaler X (1998c) Myrmecochorous dispersal distances: a world survey. J Biogeogr 25:573–580. doi: 10.1046/j.1365-2699.1998.2530573.x CrossRefGoogle Scholar
  34. Gomez C, Espadaler X, Bas JM (2005) Ant behaviour and seed morphology: a missing link of myrmecochory. Oecologia 146:244–246. doi: 10.1007/s00442-005-0200-7 PubMedCrossRefGoogle Scholar
  35. Gorb E, Gorb S (2003) Seed dispersal by ants in a deciduous forest ecosystem. Kluwer, DordrechtCrossRefGoogle Scholar
  36. Gordon DM (1983) Dependence of necrophoric response to oleic acid on social context in the ant, Pogonomyrmex badius. J Chem Ecol 9:105–111. doi: 10.1007/BF00987774 CrossRefGoogle Scholar
  37. Gove AD, Majer JD, Dunn RR (2007) A keystone ant species promotes seed dispersal in a ‘diffuse’ mutualism. Oecologia 153:687–697. doi: 10.1007/s00442-007-0756-5 PubMedCrossRefGoogle Scholar
  38. Harrington GN, Driver MA (1995) The effects of fire and ants on the seed-bank of a shrub in a semi-arid grassland. Aust J Ecol 20:538–547. doi: 10.1111/j.1442-9993.1995.tb00573.x CrossRefGoogle Scholar
  39. Hobbs RJ, Atkins L (1988) Spatial variability of experimental fires in south-west Western Australia. Aust J Ecol 13:295–299. doi: 10.1111/j.1442-9993.1988.tb00977.x CrossRefGoogle Scholar
  40. Hoffmann BD, Andersen AN (2003) Responses of ants to disturbance in Australia, with particular reference to functional groups. Aust Ecol 28:444–464. doi: 10.1046/j.1442-9993.2003.01301.x CrossRefGoogle Scholar
  41. Hughes L, Westoby M (1990) Removal rates of seeds adapted for dispersal by ants. Ecology 71:138–148Google Scholar
  42. Hughes L, Westoby M (1992a) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299. doi: 10.2307/1940676 CrossRefGoogle Scholar
  43. Hughes L, Westoby M (1992b) Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312. doi: 10.2307/1940677 CrossRefGoogle Scholar
  44. Jianmin G, Sinclair R (1993) Comparative leaf water potentials of plants in burnt and unburnt dry sclerophyll vegetation. Aust J Bot 41:661–671. doi: 10.1071/bt9930661 CrossRefGoogle Scholar
  45. Kjellsson G (1985) Seed fate in a population of Carex pilulifera L. 1. Seed dispersal and ant-seed mutualism. Oecologia 67:416–423. doi: 10.1007/BF00384949 CrossRefGoogle Scholar
  46. 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. doi: 10.1016/j.ppees.2009.08.001 CrossRefGoogle Scholar
  47. Lopez-Vila JR, Garcia-Fayos P (2005) Diplochory in Ulex parviflorus pourr. Acta Oecol 28:157–162. doi: 10.1016/j.actao.2005.03.008 CrossRefGoogle Scholar
  48. Lubertazzi D, Lubertazzi MAA, McCoy N, Gove AD, Majer JD, Dunn RR (2010) The ecology of a keystone seed disperser, the ant Rhytidoponera violacea. J Insect Sci 10:article 158)Google Scholar
  49. Lund U, Agostinelli C (2011) Circular: circular statistics. R package version 0.4-2. http://CRAN.R-project.org/package=circular
  50. Majer JD (1982) Ant–plant interaction in the Darling botanical district of Western Australia. In: Buckley RC (ed) Ant–plant interactions in Australia. Junk, London, pp 45–61CrossRefGoogle Scholar
  51. Manzaneda AJ, Rey PJ (2009) Assessing ecological specialization of an ant-seed dispersal mutualism through a wide geographic range. Ecology 90:3009–3022. doi: 10.1890/08-2274.1 PubMedCrossRefGoogle Scholar
  52. Marshall DL, Beattie AJ, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant–seed interaction. J Chem Ecol 5:335–344Google Scholar
  53. Morales MA, Heithaus ER (1998) Food from seed-dispersal mutualism shifts sex ratios in colonies of the ant Aphaenogaster rudis. Ecology 79:734–739. doi: 10.2307/176966 Google Scholar
  54. 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. doi: 10.1111/j.1600-0706.2009.17430.x CrossRefGoogle Scholar
  55. O’Dowd D, Hay ME (1980) Mutualism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 61:531–540. doi: 10.2307/1937419 CrossRefGoogle Scholar
  56. Parr CL, Andersen AN, Chastagnol C, Duffaud C (2007) Savanna fires increase rates and distances of seed dispersal by ants. Oecologia 151:33–41. doi: 10.1007/s00442-006-0570-5 PubMedCrossRefGoogle Scholar
  57. Perez B, Moreno JM (1998) Methods for quantifying fire severity in shrubland-fires. Plant Ecol 139:91–101. doi: 10.1023/A:1009702520958 CrossRefGoogle Scholar
  58. Pudlo RJ, Beattie AJ, Culver DC (1980) Population consequences of changes in an ant-seed mutualism in Sanguinaria canadensis. Oecologia 46:32–37. doi: 10.1007/BF00346962 CrossRefGoogle Scholar
  59. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org
  60. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, ChicagoGoogle Scholar
  61. Rodgerson L (1998) Mechanical defense in seeds adapted for ant dispersal. Ecology 79:1669–1677. doi:10.1890/0012-9658(1998)079[1669:MDISAF]2.0.CO;2Google Scholar
  62. Schupp EW, Jordano P, Gomez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. doi: 10.1111/j.1469-8137.2010.03402.x PubMedCrossRefGoogle Scholar
  63. Servigne P, Detrain C (2010) Opening myrmecochory’s black box: what happens inside the ant nest? Ecol Res 25:663–672. doi: 10.1007/s11284-010-0700-8 CrossRefGoogle Scholar
  64. Shattuck SO (1999) Australian ants. Their biology and identification. CSIRO, VictoriaGoogle Scholar
  65. Shea SR, McCormick J, Portlock CC (1979) Effect of fires on regeneration of leguminous species in the northern Jarrah (Eucalyptus marginata Sm) forest of Western Australia. Aust J Ecol 4:195–205. doi: 10.1111/j.1442-9993.1979.tb01210.x CrossRefGoogle Scholar
  66. Smith BH, Forman PD, Boyd AE (1989) Spatial patterns of seed dispersal and predation of two myrmecochorous forest herbs. Ecology 70:1649–1656. doi: 10.2307/1938099 CrossRefGoogle Scholar
  67. Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–385. doi: 10.1016/S0169-5347(02)02541-7 CrossRefGoogle Scholar
  68. Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114. doi: 10.1155/1958/69391 CrossRefGoogle Scholar
  69. York A (2000) Long-term effects of frequent low-intensity burning on ant communities in coastal blackbutt forests of southeastern Australia. Austral Ecol 25:83–98. doi: 10.1111/j.1442-9993.2000.tb00010.x CrossRefGoogle Scholar
  70. 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. doi: 10.1017/S0266467408004999 CrossRefGoogle Scholar
  71. Zelikova TJ, Dunn RR, Sanders NJ (2008) Variation in seed dispersal along an elevational gradient in Great Smoky Mountains National Park. Acta Oecol 34:155–162. doi: 10.1016/j.actao.2008.05.002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Kieren P. Beaumont
    • 1
    Email author
  • Duncan A. Mackay
    • 1
  • Molly A. Whalen
    • 1
  1. 1.School of Biological SciencesFlinders UniversityAdelaideAustralia

Personalised recommendations