Advertisement

Oecologia

pp 1–9 | Cite as

Ontogenetic trajectories of direct and indirect defenses of myrmecophytic plants colonized either by mutualistic or opportunistic ant species

  • Mitzi A. Fonseca-Romero
  • Juan Fornoni
  • Ek del-Val
  • Karina BoegeEmail author
Plant-microbe-animal interactions – original research

Abstract

Myrmecophytic plants are expected to produce greater direct defenses when young and switch towards indirect defenses once they reach the size and vigor to produce enough rewards for their ant mutualists. The presence of opportunistic ant species, however, is likely to promote the variation in these ontogenetic trajectories. When plants do not obtain benefits from ants, they cannot rely on this indirect defense. Hence, the expression of direct defenses is expected to remain constant or even increase during the development of plants colonized by opportunistic ants, whereas a reduction in resource allocation to indirect defenses should be observed. To assess if myrmecophytic plants adjust their ontogenetic trajectories in defense as a function of the colonizing ant species, we estimated direct and indirect defenses at four ontogenetic stages of the myrmecophytic plant Vachellia hindsii colonized by either mutualistic or opportunistic ant partners. We report that cyanogenic potential decreased while leaf thickness and the production of sugar in extrafloral nectaries increased along plant development. The magnitude of these ontogenetic changes, however, varied as a function of the identity of the colonizing ants. As expected, when colonized by opportunistic ants, plants produced more direct defenses and reduced the production of rewards. We suggest that facultative changes in the expression of ontogenetic trajectories in direct and indirect defenses could be a mechanism to reduce the fitness costs associated with opportunistic interactions.

Keywords

Exploitation Ontogenetic trajectories Plant–herbivore interactions Pseudomyrmex Vachellia 

Notes

Acknowledgements

The authors thank Rubén Pérez-Ishiwara, Omar Hernández and Rosario Razo-Belman for logistic support during fieldwork. M.F. was supported by a fellowship from Consejo Nacional de Ciencia y Tecnología (775654). This article is a requirement for the first author MFR to obtain her Master’s degree in Biological Sciences (Ecology) of the Posgrado en Ciencias Biológicas from the Universidad Nacional Autónoma de México.

Author contribution statement

MFR, JF, EV and KB conceived the ideas and designed methodology; MFR and KB conducted fieldwork, and MFR analyzed the data. MFR and KB led the writing of the manuscript. All authors contributed critically to subsequent drafts and gave final approval for its publication.

Funding

This work was funded by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica -UNAM grant (PAPIIT-IN211314) to K.B.

Compliance with ethical standards

Conflict of interest

None of the authors have any conflict of interests associated with this work.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Adler LS (2000) The ecological significance of toxic nectar. Oikos 91(3):409–420.  https://doi.org/10.1034/j.1600-0706.2000.910301.x Google Scholar
  2. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294(5541):321–326.  https://doi.org/10.1126/science.1060701 Google Scholar
  3. Agrawal AA, Rutter MT (1998) Dynamic anti-herbivore defense in ant-plants: the role of induced responses. Oikos 83:227–236Google Scholar
  4. Barton KE, Boege K (2017) Moving forward: future directions in the ontogeny of plant defense: understanding the evolutionary causes and consequences. Ecol Lett 20:403–411.  https://doi.org/10.1086/650722 Google Scholar
  5. Barton KE, Hanley ME (2013) Seedling–herbivore interactions: insights into plant defence and regeneration patterns. Ann Bot 112(4):643–650.  https://doi.org/10.1093/aob/mct139 Google Scholar
  6. Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175(4):481–493.  https://doi.org/10.1086/650722 Google Scholar
  7. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20(8):441–448.  https://doi.org/10.1016/j.tree.2005.05.001 Google Scholar
  8. Boege K, Dirzo R, Siemens D, Brown P (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10(3):177–187.  https://doi.org/10.1111/j.1461-0248.2006.01012.x Google Scholar
  9. Boege K, Agrawal A, Thaler JS (2019) Ontogenetic strategies in insect herbivores and their impact on tri-trophic interactions. Curr Opin Insect Sci 32:61–67.  https://doi.org/10.1016/j.cois.2018.11.004 Google Scholar
  10. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287.  https://doi.org/10.1046/j.1461-0248.2001.00218.x Google Scholar
  11. Bronstein JL, Alarcón R, Geber M (2006) The evolution of plant–insect mutualisms. New Phytol 172(3):412–428.  https://doi.org/10.1111/j.1469-8137.2006.01864.x Google Scholar
  12. Choong MF, Lucas PW, Ong JSY, Pereira B, Tan HTW, Turner IM (1992) Leaf fracture toughness and sclerophylly—their correlations and ecological implications. New Phytol 121:597–610Google Scholar
  13. Clark CJ, Poulsen JR, Levey DJ (2012) Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 93(3):554–564.  https://doi.org/10.1890/11-0894.1 Google Scholar
  14. Clement LW, Köppen SC, Brand WA, Heil M (2008) Strategies of a parasite of the ant–Acacia mutualism. Behav Ecol Sociobiol 62(6):953–962.  https://doi.org/10.1007/s00265-007-0520-1 Google Scholar
  15. Damián X, Fornoni J, Domínguez CA, Boege K (2018) Ontogenetic changes in the phenotypic integration and modularity of leaf functional traits. Funct Ecol 32(2):234–246.  https://doi.org/10.1111/1365-2435.12971 Google Scholar
  16. Del Val E, Dirzo R (2003) Does ontogeny cause changes in the defensive strategies of the myrmecophyte Cecropia peltata? Plant Ecol 169(1):35–41Google Scholar
  17. Del Val E, Dirzo R (2004) Mirmecofilia: las plantas con ejército propio. Interciencia 29(12):673–679Google Scholar
  18. Domínguez CA, Dirzo R (1995) Plant herbivore interactions. In: Bullock SH, Medina E, Mooney HA (eds) Mesoamerican tropical dry forests. Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 304–325Google Scholar
  19. Ferrière R, Gauduchon M, Bronstein JL (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecol Lett 10(2):115–126.  https://doi.org/10.1111/j.1461-0248.2006.01008.x Google Scholar
  20. Gianoli E, Hannunen S (2000) Plasticity of leaf traits and insect herbivory in Solanum incanum L. (Solanaceae) in Nguruman, SW Kenya. Afr J Ecol 38:183–187.  https://doi.org/10.1046/j.1365-2028.2000.00241.x Google Scholar
  21. Gómez C, Espalader X (1998) Aphaenogaster senilis Mayr (Hymenoptera, Formicidae): a possible parasite in the myrmecochory of Euphorbia characias (Euphorbiaceae). Sociobiology 32:441–450Google Scholar
  22. González-Teuber M, Bueno JCS, Heil M, Boland W (2012) Increased host investment in extrafloral nectar (EFN) improves the efficiency of a mutualistic defensive service. PLOS One.  https://doi.org/10.1371/journal.pone.0046598 Google Scholar
  23. Groom PK, Lamont BB (1999) Which common indices of sclerophylly best reflect differences in leaf structure? Écoscience 6(3):471–474.  https://doi.org/10.1080/11956860.1999.11682537 Google Scholar
  24. Guerra PC, Becerra J, Gianoli E (2010) Explaining differential herbivory in sun and shade: the case of Aristotelia chilensis saplings. Arthropod Plant Interact 4:229–234.  https://doi.org/10.1007/s11829-010-9099-y Google Scholar
  25. Heil M (2007) Indirect defence—recent developments and open questions. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in Botany, vol 69. Springer, Berlin, pp 360–395Google Scholar
  26. Heil M (2011) Nectar: generation, regulation and ecological functions. Trends Plant Sci 16(4):191–200.  https://doi.org/10.1016/j.tplants.2011.01.003 Google Scholar
  27. Heil M (2013) Let the best one stay: screening of ant defenders by Acacia host plants functions independently of partner choice or host sanctions. J Ecol 101:684–688.  https://doi.org/10.1111/1365-2745.12060 Google Scholar
  28. Heil M (2015) Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu Rev Entomol 60:213–232.  https://doi.org/10.1146/annurev-ento-010814-020753 Google Scholar
  29. Heil M, Greiner S, Meimberg H, Krüger R, Noyer JL, Heubl G, Linsenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208.  https://doi.org/10.1038/nature02703 Google Scholar
  30. Heil M, Rattke J, Boland W (2005) Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308(5721):560–563.  https://doi.org/10.1126/science.1107536 Google Scholar
  31. Heil M, Orona-Tamayo D, Eilmus S, Kautz S, González-Teuber M (2009a) Chemical communication and coevolution in an ant–plant mutualism. Chemoecology 20(2):63–74.  https://doi.org/10.1007/s00049-009-0036-4 Google Scholar
  32. Heil M, González-Teuber M, Clement LW, Kautz S, Verhaagh M, Bueno JCS (2009b) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci 106(43):18091–18096.  https://doi.org/10.1073/pnas.0904304106 Google Scholar
  33. Hernandez-Zepeda OF, Razo-Belman R, Heil M (2018) Reduced responsiveness to volatile signals creates a modular reward provisioning in an obligate food-for-protection mutualism. Front Plant Sci 9:1076.  https://doi.org/10.3389/fpls.2018.01076 Google Scholar
  34. Inouye DW (1983) The ecology of nectar robbing. In: Bentley B, Elias TS (eds) The biology of nectaries. Columbia University Press, New York, pp 153–173Google Scholar
  35. Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292.  https://doi.org/10.1146/annurev.ecolsys.110308.120330 Google Scholar
  36. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoGoogle Scholar
  37. Kautz S, Lumbsch HT, Ward PS, Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63(4):839–853.  https://doi.org/10.1111/j.1558-5646.2008.00594.x Google Scholar
  38. Kautz S, Ballhorn DJ, Kroiss J, Pauls SU, Moreau CS, Eilmus S, Heil M (2012) Host plant use by competing acacia-ants: mutualists monopolize while parasites share hosts. PLoS One.  https://doi.org/10.1371/journal.pone.0037691 Google Scholar
  39. Kitajima K, Poorter L (2010) Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytol 186(3):708–721.  https://doi.org/10.1111/j.1469-8137.2010.03212.x Google Scholar
  40. Maloof JE (2001) The effects of a bumblebee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965.  https://doi.org/10.2307/3558423 Google Scholar
  41. Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661Google Scholar
  42. Miller JT, Seigler D (2012) Evolutionary and taxonomic relationships of Acacia s.l. (Leguminosae: Mimosoideae). Aust Syst Bot 25:217–224.  https://doi.org/10.1071/SB11042 Google Scholar
  43. Ochoa-López S, Villamil N, Zedillo-Avelleyra P, Boege K (2015) Plant defense as a complex and changing phenotype throughout ontogeny. Ann Bot 1:1–10.  https://doi.org/10.1093/aob/mcv113 Google Scholar
  44. Ochoa-López S, Rebollo R, Barton KE, Fornoni J, Boege K (2018) Risk of herbivore attack and heritability of ontogenetic trajectories in plant defense. Oecologia.  https://doi.org/10.1007/s00442-018-4077-7 Google Scholar
  45. Onoda Y, Westoby M, Adler PB, Choong AM, Clissold FJ, Cornelissen JH, Díaz S, Dominy NJ, Elgart A, Enrico L, Fine PV, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Pérez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright IJ, Joseph Wright S, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312.  https://doi.org/10.1111/j.1461-0248.2010.01582.x Google Scholar
  46. Orona-Tamayo D, Heil M (2013) Stabilizing mutualisms threatened by exploiters: new insights from ant–plant research. Biotropica 45(6):654–665.  https://doi.org/10.1111/btp.12059 Google Scholar
  47. Palmer TM (2004) Wars of attrition: colony size determines competitive outcomes in a guild of African acacia ants. Anim Behav 68:993–1004.  https://doi.org/10.1016/j.anbehav.2004.02.005 Google Scholar
  48. Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci 107(40):17234–17239.  https://doi.org/10.1073/pnas.1006872107 Google Scholar
  49. Quintero C, Barton K, Boege K (2013) The ontogeny of plant indirect defenses. Perspect Plant Ecol Evol Syst 15:245–254.  https://doi.org/10.1016/j.ppees.2013.08.003 Google Scholar
  50. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
  51. Rico-Gray V (2001) Interspecific interaction. Encyclopedia of life sciences. Wiley, Hoboken, pp 1–6.  https://doi.org/10.1038/npg.els.0003280 Google Scholar
  52. Sánchez Galván IR, Rico-Gray V (2011) La fuerza del amor en el Neotrópico: contraste en la eficiencia defensiva de dos especies de hormigas del género Pseudomyrmex sobre plantas de Acacia cornígera (Parte II). Cuadernos de Biodiversidad 36:10–16Google Scholar
  53. Schappert PJ, Shore JS (1995) Cyanogenesis in Turnera ulmifolia L. (Turneraceae). I. Phenotypic distribution and genetic variation for cyanogenesis on Jamaica. Heredity 74:392–404.  https://doi.org/10.1038/hdy.1995.57 Google Scholar
  54. Schmid B, Puttick GM, Bazzaz FA (1988) Clonal integration and effects of simulated herbivory in old-field perennials. Oecologia 75:465–471.  https://doi.org/10.1007/BF00376953 Google Scholar
  55. Seigler DS (1991) Cyanide and cyanogenic glycosides. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Vol I The chemical participants, vol 2. Academic Press, New York, pp 35–77Google Scholar
  56. Seigler DS, Ebinger JE (1987) Cyanogenic glycosides in ant-acacias of Mexico and Central America. Southwest Nat.  https://doi.org/10.2307/3671484 Google Scholar
  57. Smith FA, Smith SE (1996) Mutualism and parasitism: diversity in function and structure in the “arbuscular” (VA) mycorrhizal symbiosis. Adv Bot Res 22:1–43.  https://doi.org/10.1016/s0065-2296(08)60055-5 Google Scholar
  58. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78(1):23–55.  https://doi.org/10.1086/367580 Google Scholar
  59. Villamil N, Márquez-Guzmán J, Boege K (2013) Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries. Ann Bot 112:701–709.  https://doi.org/10.1093/aob/mct005 Google Scholar
  60. Ward PS, Downie DA (2005) The ant subfamily Pseudomyrmecinae (Hymenoptera: Formicidae): phylogeny and evolution of big-eyed arboreal ants. Syst Entomol 30(2):310–335.  https://doi.org/10.1111/j.1365-3113.2004.00281.x Google Scholar
  61. Westbrook JW, Kitajima K, Burleigh JG, Kress WJ, Erickson DL, Wright SJ (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a neotropical forest. Am Nat 177(6):800–811.  https://doi.org/10.1086/659963 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  2. 2.Posgrado en Ciencias Biológicas, Unidad de Posgrado Edificio A, 1° Piso, Circuito de PosgradosCiudad Universitaria, CoyoacánMexico CityMexico
  3. 3.Instituto de Investigaciones en Ecosistemas y SustentabilidadUniversidad Nacional Autónoma de MéxicoMoreliaMexico
  4. 4.Escuela Nacional de Estudios Superiores Unidad MoreliaUniversidad Nacional Autónoma de MéxicoMoreliaMexico

Personalised recommendations