Advertisement

Ants Associated with Turnera subulata (Turneraceae): Elaiosome Attraction, Seed Dispersion and Germination

  • M L C Rocha
  • P F Cristaldo
  • J S Cruz
  • J J M Sacramento
  • D V Ferreira
  • A P A Araújo
Ecology, Behavior and Bionomics

Abstract

Symbiosis between plants and ants include examples in which the plant provides shelter and/or food for ants that, in turn, act in the defense or in the dispersion of seeds from the host plant. Although traditionally referred as mutualistic, the results of these interactions may vary with the ecological context in which patterns are involved. A range of species have facultative association with Turnera subulata (Turneraceae). Here, using behavioral bioassays, we investigated the effects of the most frequent ant species associated with T. subulata (Brachymyrmex sp.1, Camponotus blandus (Smith), Dorymyrmex sp.1, Crematogaster obscurata Emery, and Solenopsis invicta Buren) in the dispersion of plant host seeds and in the number of seedlings around the associated ant nests. We also evaluated the effects of these ant species in the germination of T. subulata seeds, in the consumption of elaiosome, and in the attractiveness to elaiosome odor. Our results showed that the ant species associated with T. subulata presented variation in the attraction by the odor and in the rate of consumption of the elaiosomes. However, none of the ant species studied contributed significantly to the increase of seed germination and seedling growth. Our results suggest that the consumption of the elaiosome by ant species is not a determinant factor to the success of germination of T. subulata. However, such species could contribute indirectly to seed germination by carrying seeds to sites more fertile to germination. In general, our results help to elucidate the results of ecological interactions involving ants and plants.

Keywords

Myrmecochory plant-ant context-dependent symbiosis 

Supplementary material

13744_2018_616_MOESM1_ESM.docx (88 kb)
ESM 1 (DOCX 88 kb)

References

  1. Arbo MM (2005) Estudios sistemáticos en Turnera (Turneraceae). III Series Anomalae y Turnera Bonplandia 14:115–318Google Scholar
  2. Arbo MM (2013) Turneraceae. In: Prata AP, Amaral MC, Farias MC, Alves MV (eds) Flora de Sergipe. Gráfica e Editora Triunfo, Aracaju, pp 533–459Google Scholar
  3. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge, New YorkCrossRefGoogle Scholar
  4. Beattie AJ, Hughes L (2002) Ant-plant interactions. In: Herrera CM, Pellmyr O (eds) Plant-animal interaction. Blackwell Publishing, Oxford, pp 211–235Google Scholar
  5. Benitez-Vieyra S, Ordano M, Fornoni J et al (2010) Selection on signal–reward correlation: limits and opportunities to the evolution of deceit in Turnera ulmifolia L. J Evol Biol 23:2760–2767.  https://doi.org/10.1111/j.1420-9101.2010.02132.x CrossRefPubMedGoogle Scholar
  6. Bøhn T, Amundsen P-A (2004) Ecological interactions and evolution: forgotten parts of biodiversity? Biosci 54:804–805. https://doi.org/10.1641/0006-3568(2004)054[0804:EIAEFP]2.0.CO;2Google Scholar
  7. Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217CrossRefPubMedGoogle Scholar
  8. Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant–insect mutualisms. New Phytol 172:412–428.  https://doi.org/10.1111/j.1469-8137.2006.01864.x CrossRefPubMedGoogle Scholar
  9. Chamberland SA, Holland JN (2009) Quantitative synthesis of context dependency in ant – plant protection mutualisms. Ecology 90:2384–2392CrossRefGoogle Scholar
  10. Chlumský J, Koutecký P, Jílková V, Štech M (2012) Roles of species-preferential seed dispersal by ants and endozoochory in Melampyrum (Orobanchaceae). J Plant Ecol 6:232–239.  https://doi.org/10.1093/jpe/rts039 CrossRefGoogle Scholar
  11. Christian CE, Stanton ML (2004) Cryptic consequences of a dispersal mutualism: seed burial, elaiosome removal, and seed-bank dynamics. Ecology 85:1101–1110.  https://doi.org/10.1890/03-0059 CrossRefGoogle Scholar
  12. Crawley MJ (2012) The R book. John Wiley & Sons Ltd, HobokenCrossRefGoogle Scholar
  13. Cruz NG, Cristaldo PF, Bacci L, Almeida CS, Camacho GP, Santana AS, Ribeiro EJM, Oliveira AP, Santos AA, Araújo APA (2018) Variation in the composition and activity of ants on defense of host plant Turnera subulata (Turneraceae): strong response to simulated herbivore attacks and to herbivore’s baits. Arthropod Plant Interact 12:113–121.  https://doi.org/10.1007/s11829-017-9559-8 CrossRefGoogle Scholar
  14. Di Gusto B, Anstett GM, Dounias E, McKey DB (2001) Variation in the effectiveness of biotic defence: the case of an opportunistic ant-plant protection mutualism. Oecologia 129:367–375.  https://doi.org/10.1007/s004420100734 CrossRefGoogle Scholar
  15. Edwards DP, Yu DW (2007) The roles of sensory traps in the origin, maintenance, and breakdown of mutualism. Behav Ecol Sociobiol 61:1321–1327.  https://doi.org/10.1007/s00265-007-0369-3 CrossRefGoogle Scholar
  16. 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. Insect Soc 52:55–62.  https://doi.org/10.1007/s00040-004-0773-x CrossRefGoogle Scholar
  17. 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.  https://doi.org/10.1007/s00442-007-0931-8 CrossRefPubMedGoogle Scholar
  18. Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers Conserv 7:1221–1244.  https://doi.org/10.1023/A:1008891901953 CrossRefGoogle Scholar
  19. Gammans N, Bullock JM, Schönrogge K (2005) Ant benefits in a seed dispersal mutualism. Oecologia 146:43–49.  https://doi.org/10.1007/s00442-005-0154-9 CrossRefPubMedGoogle Scholar
  20. Gibson W (1993) Selective advantages to hemi-parasitic annuals, genus Melampyrum, of a seed-dispersal mutualism involving ants: I. Favorable nest sites. Oikos 67:334–344.  https://doi.org/10.2307/3545480 CrossRefGoogle Scholar
  21. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492.  https://doi.org/10.1111/j.0030-1299.2006.14258.x CrossRefGoogle Scholar
  22. Gómez C, Espadaler X, Bas JM (2005) Ant behaviour and seed morphology: a missing link of myrmecochory. Oecologia 146:244–246.  https://doi.org/10.1007/s00442-005-0200-7 CrossRefPubMedGoogle Scholar
  23. Heil M, Mckey D (2003) Protective ant-plant interactions as models system in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453.  https://doi.org/10.1146/annurev.ecolsys.34.011802.132410 CrossRefGoogle Scholar
  24. Hughes L, Westoby M (1992) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299.  https://doi.org/10.2307/1940676 CrossRefGoogle Scholar
  25. Hughes L, Westoby M, Jurado E (1994) Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition. Funct Ecol 8:358–365.  https://doi.org/10.2307/2389829 CrossRefGoogle Scholar
  26. Inouye DW, Taylor OR (1979) A temperate region plant-ant-seed predator system: consequences of extra floral nectar secretion by Helianthella quinquenervis. Ecology 60:2–7.  https://doi.org/10.2307/1936460 CrossRefGoogle Scholar
  27. Janzen DH (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution (N Y) 20:249–275.  https://doi.org/10.2307/2406628 CrossRefGoogle Scholar
  28. Leal IR, Wirth R, Tabarelli M (2007) Seed dispersal by ants in the semi-arid caatinga of north-East Brazil. Ann Bot 99:885–894.  https://doi.org/10.1093/aob/mcm017 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Leal LC, Neto MCL, de Oliveira AFM, Andersen AN, Leal IR (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.  https://doi.org/10.1007/s00442-013-2789-2 CrossRefPubMedGoogle Scholar
  30. O’Dowd DJ, Hay ME (1980) Multalism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 61:531–540.  https://doi.org/10.2307/1937419 CrossRefGoogle Scholar
  31. Passos L, Oliveira PS (2003) Interactions between ants, fruits and seeds in a restinga forest in South-Eastern Brazil. J Trop Ecol 19:261–270.  https://doi.org/10.1017/S0266467403003298 CrossRefGoogle Scholar
  32. Pfeiffer M, Huttenlocher H, Ayasse M (2010) Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants. Funct Ecol 24:545–555.  https://doi.org/10.1111/j.1365-2435.2009.01661.x CrossRefGoogle Scholar
  33. Pires LP, Del-Claro K (2014) Variation in the outcomes of an ant-plant system: fire and leaf fungus infection reduce benefits to plants with extrafloral nectaries. J Insect Sci 14:84.  https://doi.org/10.1093/jis/14.1.84
  34. Prata A, Amaral M, Farias M, Alves M (2013) Flora de Sergipe, vol. 1. Editora Triunfo, Aracaju, p 592Google Scholar
  35. R Development Core Team (2016) R: a language and environment for statistical computing. The R foundation for statistical computing. Vienna, Austria, ISBN: 3-900051-07-0Google Scholar
  36. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  37. Sheridan SL, Iversen KA, Itagaki H (1996) The role of chemical senses in seed-carrying behavior by ants: a behavioral, physiological, and morphological study. J Insect Physiol 42:149–159.  https://doi.org/10.1016/0022-1910(95)00087-9 CrossRefGoogle Scholar
  38. Tanaka K, Ogata K, Mukai H, Yamawo A, Tokuda M (2015) Adaptive advantage of myrmecochory in the ant-dispersed herb Lamium amplexicaule (Lamiaceae): predation avoidance through the deterrence of post-dispersal seed predators. PLoS One 10:e0133677.  https://doi.org/10.1371/journal.pone.0133677 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Turner KM, Frederickson ME (2013) Signals can trump rewards in attracting seed-dispersing ants. PLoS One 8:e71871CrossRefPubMedPubMedCentralGoogle Scholar
  40. Whitney KD (2002) Dispersal for distance? Acacia ligulata seeds and meat ants Iridomyrmex viridiaeneus. Austral Ecol 27:589–595.  https://doi.org/10.1046/j.1442-9993.2002.01216.x CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2018

Authors and Affiliations

  • M L C Rocha
    • 1
    • 2
  • P F Cristaldo
    • 1
    • 3
  • J S Cruz
    • 1
  • J J M Sacramento
    • 1
  • D V Ferreira
    • 1
    • 2
  • A P A Araújo
    • 1
  1. 1.Lab de Interações Ecológicas, Depto de EcologiaUniv Federal de SergipeSão CristóvãoBrasil
  2. 2.Programa de Pós-Graduação em Ecologia e ConservaçãoUniv Federal de SergipeSão CristóvãoBrasil
  3. 3.Programa de Pós-Graduação em Agricultura e BiodiversidadeUniv Federal de SergipeSão CristóvãoBrasil

Personalised recommendations