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Oecologia

pp 1–12 | Cite as

Tasty rewards for ants: differences in elaiosome and seed metabolite profiles are consistent across species and reflect taxonomic relatedness

  • Marie Konečná
  • Martin Moos
  • Helena Zahradníčková
  • Petr Šimek
  • Jan Lepš
Population ecology – original research

Abstract

Diaspores of myrmecochorous plants consist of a seed (or fruit) and an attached appendage (elaiosome) which attracts ants. The elaiosome is a food resource for ants, whereas the seed is an energy source for subsequent germination and plant establishment. Although myrmecochory occurs in many phylogenetically unrelated lineages, multiple phylogenetic lineages display similar variation in elaiosome and seed metabolite composition due to convergent evolution. We focused on four families (Amaryllidaceae, Boraginaceae, Papaveraceae and Poaceae) each represented by two species from different genera. Diaspores of three populations per species were sampled and concentrations of 60 metabolites from five groups (amino acids, fatty acids, organic acids, polyols and sugars) were determined for both elaiosomes and seeds. Variability in metabolite composition was decomposed by hierarchical ANOVA and variation partitioning using redundancy analysis (reflecting both species nested within families, crossed with seed vs. elaiosome). Differences in the metabolite composition of elaiosomes and seeds were consistent across multiple phylogenetic origins (with more pronounced differences at the level of individual metabolites than at the level of metabolite groups) and supported the idea of convergent evolution under strong selection pressure. Elaiosomes contained higher amounts of easily digestible metabolites (especially amino acids) than seeds. Fatty acids were not more concentrated in elaiosomes, which contradicts the literal translation of “elaiosome” (= oil body). The differentiation of metabolite composition closely reflected taxonomic relatedness, particularly at the family level. Differences among populations within species were small, so the metabolite composition can thus be considered as a trait with relatively low intraspecific variability.

Keywords

Myrmecochory Convergent evolution Variation partitioning Ant–plant mutualism Seed dispersal 

Notes

Acknowledgements

Anna Heydova is gratefully acknowledged for skilled analytical sample preparation, Conor Redmond for editing our English and Pavel Fibich for the help with drawing figures in R. The research was supported by the Czech Science Foundation—GACR 14-36079G—PLADIAS.

Author contribution statement

MK and JL designed the experiment, MK collected the plant diaspores and prepared separated samples of elaisomes and seeds, MM and HZ conducted the chemical analyses, MK and JL carried out the statistical analyses. MK wrote the first draft of the manuscript with JL, and MM, HZ and PŠ contributed the chemical aspects. All the authors revised the text and agreed upon the final version.

Supplementary material

442_2018_4254_MOESM1_ESM.doc (679 kb)
Supplementary material 1 (DOC 679 kb)

References

  1. Boieiro M, Espadaler X, Gomez C, Eustaquio A (2012) Spatial variation in the fatty acid composition of elaiosomes in an ant-dispersed plant: differences within and between individuals and populations. Flora 207:497–502.  https://doi.org/10.1016/j.flora.2012.06.007 CrossRefGoogle Scholar
  2. Boulay R, Coll-Toledano J, Cerda X (2006) Geographic variations in Helleborus foetidus elaiosome lipid composition: implications for dispersal by ants. Chemoecology 16:1–7.  https://doi.org/10.1007/s00049-005-0322-8 CrossRefGoogle Scholar
  3. Bresinsky A (1963) Bau, Entwicklungsgeschichte und Inhaltsstoffe der Elaiosomen. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 1–54Google Scholar
  4. Bresinsky A (2014) Ants, plants and fungi: a view on some patterns of interaction and diversity. In: Lüttge U, Beyschlag W, Progress in botany 75. Springer-Verlag, Berlin Heidelberg, pp 3–54. https://doi.org/10.1007/978-3-642-38797-5_1Google Scholar
  5. Brew CR, O’Dowd DJ, Rae ID (1989) Seed dispersal by ants—behaviour-releasing compounds in elaiosomes. Oecologia 80:490–497.  https://doi.org/10.1007/BF00380071 CrossRefPubMedGoogle Scholar
  6. Canner JE, Dunn RR, Giladi I, Gross K (2012) Redispersal of seeds by a keystone ant augments the spread of common wildflowers. Acta Oecol Int J Ecol 40:31–39.  https://doi.org/10.1016/j.actao.2012.02.004 CrossRefGoogle Scholar
  7. Chen G, Huang S-Z, Chen S-C, Chen Y-H, Liu X, Sun W-B (2016) Chemical composition of diaspores of the myrmecochorous plant Stemona tuberosa Lour. Biochem Syst Ecol 64:31–37.  https://doi.org/10.1016/j.bse.2015.11.009 CrossRefGoogle Scholar
  8. Ciccarelli D, Andeucci AC, Pagni AM, Garbari F (2005) Structure and development of the elaiosome in Myrtus communis L. (Myrtaceae) seeds. Flora 200:326–331.  https://doi.org/10.1016/j.flora.2004.12.004 CrossRefGoogle Scholar
  9. Diez JM, Giladi I, Warren R, Pulliam HR (2014) Probabilistic and spatially variable niches inferred from demography. J Ecol 102:544–554.  https://doi.org/10.1111/1365-2745.12215 CrossRefGoogle Scholar
  10. Dunn RR, Gove AD, Barraclough TG, Givnish TJ, Majer JD (2007) Convergent evolution of an ant–plant mutualism across plant families, continents, and time. Evol Ecol Res 9:1349–1362Google Scholar
  11. 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.  https://doi.org/10.1007/s00040-004-0773-x CrossRefGoogle Scholar
  12. Fischer RC, Richter A, Hadacek F, Mayer V (2008) Chemical diferences 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
  13. Gammans N, Bullock JM (2006) Reaction of mutualistic and granivorous ants to Ulex elaiosome chemicals. J Chem Ecol 32:1935–1947.  https://doi.org/10.1007/s10886-006-9119-7 CrossRefPubMedGoogle Scholar
  14. 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
  15. 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
  16. Gorb EV, Gorb SN (2003) Seed dispersal by ants in a deciduous forest ecosystem. Kluwer academic publishers, Dordrecht, NetherlandsCrossRefGoogle Scholar
  17. Heithaus ER (1981) Seed predation by rodents on three ant-dispersed plants. Ecology 62:136–145.  https://doi.org/10.2307/1936677 CrossRefGoogle Scholar
  18. 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
  19. Košťál V, Doležal R, Rozsypal J, Moravcová M, Zahradníčková H, Šimek P (2011a) Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. J Insect Physiol 57:1136–1146.  https://doi.org/10.1016/j.jinsphys.2011.03.011 CrossRefPubMedGoogle Scholar
  20. Košťál V, Zahradníčková H, Šimek P (2011b) Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen. PNAS 108:13041–13046.  https://doi.org/10.1073/pnas.1107060108 CrossRefPubMedGoogle Scholar
  21. Lanza J, Schmitt MA, Awad AB (1992) Comparative chemistry of elaiosomes of 3 species of Trillium. J Chem Ecol 18:209–221.  https://doi.org/10.1007/BF00993754 CrossRefPubMedGoogle Scholar
  22. 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.  https://doi.org/10.1016/j.ppees.2009.08.001 CrossRefGoogle Scholar
  23. Lepš J, de Bello F, Šmilauer P, Doležal J (2011) Community trait response to environment: disentangling species turnover vs intraspecific trait variability effects. Ecography 34:856–863.  https://doi.org/10.1111/j.1600-0587.2010.06904.x CrossRefGoogle Scholar
  24. Lopez-Riquelme GO, Malo EA, Cruz-Lopez L, Fanjul-Moles ML (2006) Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (Hymenoptera: Formicidae). Physiol Entomol 31:353–360.  https://doi.org/10.1111/j.1365-3032.2006.00526.x CrossRefGoogle Scholar
  25. Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersed seeds. Oecologia 107:95–101.  https://doi.org/10.1007/BF00582239 CrossRefPubMedGoogle Scholar
  26. Mayer V, Svoma E (1998) Development and function of the elaiosome in Knautia (Dipsacaceae). Bot Acta 111:402–410.  https://doi.org/10.1111/j.1438-8677.1998.tb00726.x CrossRefGoogle Scholar
  27. Mayer V, Ölzant S, Fischer RC (2005) Myrmecochorous seed dispersal in temperate regions. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate predation, dispersal and seedling establishment. CABI Publishing, Wallingford, p 175–196Google Scholar
  28. Peternelli EFD, Barbosa LCA, Della Lucia TMC (2008) Isolation of compounds attractive to the leaf-cutting ant Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) from Mabea fistulifera elaiosome. Quim Nova 31:475–478.  https://doi.org/10.1590/S0100-40422008000300002 CrossRefGoogle Scholar
  29. 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
  30. Reifenrath K, Becker Ch, Poethke JH (2012) Diaspore trait preferences of dispersing ants. J Chem Ecol 38:1093–1104.  https://doi.org/10.1007/s10886-012-0174-y CrossRefPubMedGoogle Scholar
  31. Schmeer K, Nicholson G, Zhang S, Bayer E, Bohning-Gaese K (1996) Identification of the lipids and the ant attractant 1,2-dioleolglycerol in the arils of Commiphora guillaumini Perr. (Burseraceae) by supercritical fluid chromatography-atmospheric pressure chemical ionisation mass spektrometry. J Chromatogr 727:139–146CrossRefGoogle Scholar
  32. Sernander R (1906) Entwurf einer Monographie der europäischen Myrmekochoren. Kungliga Svenska Vetenskapsakademiens Handlingar 41:1–410Google Scholar
  33. Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using Canoco 5. Cambridge University Press, Cambridge, pp 1–362. https://doi.org/10.1017/cbo9781139627061Google Scholar
  34. Stevens PF (2016) Angiosperm Phylogeny Website. Version 13. http://www.mobot.org/MOBOT/research/APweb/. Accessed 4 Sept 2016
  35. ter Braak CJF, Šmilauer P (2012) CANOCO Reference manual and User´s guide: Software for ordination (version 5.0). Microcomputer Power, Ithaca, pp 1–496Google Scholar
  36. Turner KM, Frederickson ME (2013) Signals can trumpt rewards in attracting seed-dispersing ants. PLoS One 8:1–8.  https://doi.org/10.1371/journal.pone.0071871 CrossRefGoogle Scholar
  37. Zahradníčková H, Tomčala A, Berková P, Schneedorferová I, Okrouhlík J, Šimek P, Hodková M (2014) Cost effective, robust, and reliable coupled separation techniques for the identification and quantification of phospholipids in complex biological matrices: application to insects. J Sep Sci 37:2062–2068.  https://doi.org/10.1002/jssc.201400113 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Biology CentreCzech Academy of SciencesČeské BudějoviceCzech Republic

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