Skip to main content
SpringerLink
Log in

Dispersal mechanisms of the narrow endemic Polygala vayredae: dispersal syndromes and spatio-temporal variations in ant dispersal assemblages

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

This study assesses the dispersal mechanisms of the narrow endemic Polygala vayredae, analysing the functioning of its dispersal syndromes (anemochory and myrmecochory), the spatio-temporal variability of the disperser assemblage, foraging behaviour and dispersal ability, and the role of the elaiosome in ant attraction and seed germination. The dispersion of diaspores begins when either (1) capsules or seeds fall beneath the mother plant (barochory) or (2) the seeds are directly collected in the suspended capsules by ants (myrmecochory). As capsules frequently open and expose/disseminate seeds before leaving the mother plant, the adaptation for anemochory appears to be reduced and rarely functional, possibly with only occasional events of long-distance dispersal (e.g. under extreme weather conditions). P. vayredae is essentially myrmecochorous and a diverse array of ant species are involved in seed manipulation, with the elaiosome playing a major role in ant attraction. From the plant’s perspective for dispersal, the majority of ant species had a positive interaction with the seeds, but negative and potential neutral interactions were also observed. Overall, dispersal distances were limited and were mainly determined by ant body size. The frequency of interactions and the ant assemblage varied significantly both spatially and temporally, and these factors may have an effect on directing or disrupting the selection of plant traits. Low seed predation and similar germination rates of intact seeds compared with seeds without elaiosome indicate that seed predator avoidance and seed germination improvement after ant manipulation are not among the selective advantages of myrmecochory operating at present. Dispersal mechanisms that enhance seed dispersal within the population and only occasionally lead to long-distance dispersal events, along with the rarity and patchiness of suitable habitats, may be the main factors explaining the actual density and narrow distribution of this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alcántara JM, Rey PJ, Manzaneda AJ, Boulay R, Ramírez JM, Fedriani JM (2007) Geographic variation in the adaptive landscape for seed size at dispersal in the myrmecochorous Helleborus foetidus. Evol Ecol 21:411–430

    Article  Google Scholar 

  • Andersen AN (1992) Regulation of ‘momentary’ diversity by dominant species in exceptionally rich ant communities of the Australian seasonal tropics. Am Nat 140:401–420

    Article  CAS  PubMed  Google Scholar 

  • Andersen AN, Majer JD (2004) Ants show the way down under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298

    Article  Google Scholar 

  • Beattie A (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge

    Google Scholar 

  • Berg RY (1975) Myrmecochorous plants in Australia and their dispersal by ants. Aust J Bot 23:475–508

    Article  Google Scholar 

  • Bolós A (1946) La Polygala vayredae Costa, endemismo pirenaico. Collect Bot 1:7–93

    Google Scholar 

  • Boulay R, Coll-Toledano J, Cerdá X (2006) Geographic variations in Helleborus foetidus elaiosome lipid composition: implications for dispersal by ants. Chemoecology 16:1–7

    Article  CAS  Google Scholar 

  • Boulay R, Carro F, Soriguer RC, Cerdá X (2007) Synchrony between fruit maturation and effective dispersers’ foraging activity increases seed protection against seed predators. Proc R Soc Biol Sci Ser B 274:2515–2522

    Article  Google Scholar 

  • Boyd RS (2001) Ecological benefits of myrmecochory for the endangered chaparral shrub Fremontodendron decumbens (Sterculiaceae). Am J Bot 88:234–241

    Article  PubMed  Google Scholar 

  • Castro S (2007) Reproductive biology and conservation of the endemic Polygala vayredae. PhD Dissertation, University of Aveiro

  • Castro S, Silveira P, Navarro L (2008) How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Bot J Linn Soc 157:67–81

    Article  Google Scholar 

  • Castro S, Silva S, Stanescu I, Silveira P, Navarro L, Santos C (2009a) Pistil anatomy and pollen tube development in Polygala vayredae Costa (Polygalaceae). Plant Biol 11:405–416

    Article  CAS  PubMed  Google Scholar 

  • Castro S, Silveira P, Navarro L (2009b) Floral traits variation, legitimate pollination, and nectar robbing in Polygala vayredae (Polygalaceae). Ecol Res 24:47–55

    Article  Google Scholar 

  • Cerdá X, Retana J, Manzaneda A (1998) The role of competition by dominants and temperature in the foraging of subordinate species in Mediterranean ant communities. Oecologia 117:404–412

    Article  Google Scholar 

  • Culver DC, Beattie AJ (1978) Myrmecochory in Viola: dynamics of seed-ant interactions in some West Virginia species. J Ecol 66:53–72

    Article  Google Scholar 

  • Culver DC, Beattie AJ (1980) The fate of Viola seeds dispersed by ants. Am J Bot 67:710–714

    Article  Google Scholar 

  • Edwards W, Dunlop M, Rodgerson L (2006) The evolution of rewards: seed dispersal, seed size and elaiosome size. J Ecol 94:687–694

    Article  Google Scholar 

  • Feener DH, Schupp EW (1998) Effect of treefall gaps on the patchiness and species richness of Neotropical ant assemblages. Oecologia 116:191–201

    Article  Google Scholar 

  • Forest F, Chase MW, Persson C, Crane PR, Hawkins JA (2007) The role of biotic and abiotic factors in evolution of ant dispersal in the milkwort family (Polygalaceae). Evolution 61:1675–1694

    Article  CAS  PubMed  Google Scholar 

  • Gammans N, Bullock JM, Schönrogge K (2005) Ant benefits in a seed dispersal mutualism. Oecologia 146:43–49

    Article  PubMed  Google Scholar 

  • Garrido JL, Rey PJ, Cerdá X, Herrera CM (2002) Geographical variation in diaspore traits of an ant-dispersed plant (Helleborus foetidus): are ant community composition and diaspore traits correlated? J Ecol 90:446–455

    Article  Google Scholar 

  • Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492

    Article  Google Scholar 

  • Gómez 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

    Article  Google Scholar 

  • Gómez C, Espadaler X (1998b) Myrmecochorous dispersal distances: a world survey. J Biogeogr 25:573–580

    Article  Google Scholar 

  • Gómez C, Pons P, Bas JM (2003) Effects of the argentine ant Linepithema humile on seed dispersal and seedling emergence of Rhamnus alaternus. Ecography 26:532–538

    Article  Google Scholar 

  • Gorb E, Gorb S (2003) Seed dispersal by ants in a deciduous forest ecosystem. Kluwer Academic Publishers, Dordrecht, Boston, London

    Google Scholar 

  • Guitián J, Garrido JL (2006) Is early flowering in myrmecochorous plants an adaptation for ant dispersal? Plant Species Biol 21:165–171

    Article  Google Scholar 

  • Guitián P, Medrano M, Guitián J (2003) Seed dispersal in Erythronium dens-canis L. (Liliaceae): variation among habitats in a myrmecochorous plant. Plant Ecol 169:171–177

    Article  Google Scholar 

  • Handel SN (1978) Competitive relationship of three woodland sedges and its bearing on evolution of ant-dispersal of Carex pedunculata. Evolution 32:151–163

    Article  Google Scholar 

  • Heithaus ER (1981) Seed predation by rodents on three ant-dispersed plants. Ecology 62:136–145

    Article  Google Scholar 

  • Higashi S, Tsuyuzaki S, Ohara M, Ito F (1989) Adaptive advantages of ant-dispersed seeds in the myrmecochorous plant Trillium tschonoskii (Liliaceae). Oikos 54:389–394

    Article  Google Scholar 

  • Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Horvitz CC, Schemske DW (1986) Ant-nest soil and seedling growth in a neotropical ant-dispersed herb. Oecologia 70:318–320

    Article  Google Scholar 

  • Hughes L, Westoby M (1992a) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299

    Article  Google Scholar 

  • Hughes L, Westoby M (1992b) Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312

    Article  Google Scholar 

  • Hughes L, Westoby M, Jurado E (1994) Convergence of elaiosomes and insect prey: evidence from ant foraging behavior and fatty acid composition. Funct Ecol 8:358–365

    Article  Google Scholar 

  • Imbert E (2006) Dispersal by ants in Centaurea corymbosa (Asteraceae): what is the elaiosome for? Plant Species Biol 21:109–117

    Article  Google Scholar 

  • Lack AJ, Kay QON (1987) Genetic structure, gene flow and reproductive ecology in sand-dune populations of Polygala vulgaris. J Ecol 75:259–276

    Article  Google Scholar 

  • Lanza J, Schmitt MA, Awad AB (1992) Comparative chemistry of elaiosomes of 3 species of Trillium. J Chem Ecol 18:209–221

    Article  CAS  Google Scholar 

  • Lassau SA, Hochuli DF (2004) Effects of habitat complexity on ant assemblages. Ecography 27:157–164

    Article  Google Scholar 

  • Lesica P, Yurkewycz R, Crone EE (2006) Rare plants are common where you find them. Am J Bot 93:454–459

    Article  Google Scholar 

  • Manzaneda AJ, Rey PJ (2009) Assessing ecological specialization of an ant-seed dispersal mutualism through a wide geographic range. Ecology

  • Manzaneda AJ, Fedriani JM, Rey PJ (2005) Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range. Ecography 28:583–592

    Article  Google Scholar 

  • Manzaneda AJ, Rey PJ, Boulay R (2007) Geographic and temporal variation in the ant-seed dispersal assemblage of the perennial herb Helleborus foetidus L. (Ranunculaceae). Biol J Linn Soc 92:135–150

    Article  Google Scholar 

  • Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersed seeds. Oecologia 107:95–101

    Article  Google Scholar 

  • Morales MA, Heithaus ER (1998) Food from seed dispersal mutualism shifts sex ratios in colonies of the ant Aphaenogaster rudis. Ecology 79:734–739

    Google Scholar 

  • Münzbergova Z (2004) Effect of spatial scale on factors limiting species distributions in dry grassland fragments. J Ecol 92:854–867

    Article  Google Scholar 

  • Nathan R, Sapir N, Trakhtenbrot A, Katul GG, Bohrer G, Otte M, Avissar R, Soons MB, Horn HS, Wikelski M, Levin SA (2005) Long-distance biological transport processes through the air: can nature’s complexity be unfolded in silico? Divers Distrib 11:131–137

    Article  Google Scholar 

  • Navarro L, Guitián J (2003) Seed germination and seedling survival of two threatened endemic species of the northwest Iberian Peninsula. Biol Conserv 109:313–320

    Article  Google Scholar 

  • Ness JH, Morin DF (2008) Forest edges and landscape history shape interactions between plants, seed-dispersing ants and seed predators. Biol Conserv 141:838–847

    Article  Google Scholar 

  • Ness JH, Bronstein JL, Andersen AN, Holland JN (2004) Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions. Ecology 85:1244–1250

    Article  Google Scholar 

  • Oberrath R, Bohning-Gaese K (2002) Phenological adaptations of ant-dispersed plants to seasonal variation in ant activity. Ecology 83:1412–1420

    Article  Google Scholar 

  • Oostermeijer JGB (1989) Myrmecochory in Polygala vulgaris L., Luzula campestris (L.) DC. and Viola curtisii Forster in a Dutch dune area. Oecologia 78:302–311

    Article  Google Scholar 

  • Retana J, Cerdá X (2000) Patterns of diversity and composition of Mediterranean ground ant communities: tracking spatial and temporal variability in the thermal environment. Oecologia 123:436–444

    Article  Google Scholar 

  • Rey PJ, Manzaneda AJ (2007) Geographical variation in the determinants of seed dispersal success of a myrmecochorous herb. J Ecol 95:1381–1393

    Article  Google Scholar 

  • Rey PJ, Ramírez JM, Sánchez-Lafuente AM (2006) Seed- vs. micro-site limited recruitment in a myrmecochorous herb. Plant Ecol 184:213–222

    Article  Google Scholar 

  • Rico-Gray V, García-Franco JG, Palacios-Rios M, Díaz-Castelazo C, Parra-Tabla V, Navarro JA (1998) Geographical and seasonal variation in the richness of ant-plant interactions in México. Biotropica 30:190–200

    Article  Google Scholar 

  • Sernander R (1906) Entwurf einer Monographie der Europaischen Myrmekochoren. K Sv Vetensk Akad Handl 41:1–140

  • Thompson JN (1994) The geographic mosaic of evolving interactions. In: Leather SR, Watt AD, Mills NJ, Walters KFA (eds) Individuals, populations and patterns in ecology. Intercept Press, Andover

    Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • van der Pijl L (1982) Principles of dispersal in higher plants. Springer-Verlag, Berlin, Heidelberg, New York

    Google Scholar 

  • Van Der Veken S, Rogister J, Verheyen K, Hermy M, Nathan RAN (2007) Over the (range) edge: a 45-year transplant experiment with the perennial forest herb Hyacinthoides non-scripta. J Ecol 95:343–351

    Article  Google Scholar 

  • van Roosmalen MGM (1985) Fruits of the Guianan flora. Utrecht University, Utecht

    Google Scholar 

Download references

Acknowledgements

The authors thank the Departament de Medi Ambient of Generalitat de Catalunya and the Consorci d’Alta Garrotxa for allowing this research and Parc Natural de la Zona Volcànica de la Garrotxa for all the assistance, namely Mònica Canal for field support. Kiko Gómez is also thanked for the photographs of ant specimens. The Portuguese Foundation for Science and Technology financed the work of Sílvia Castro (BD/10901/2002 and BPD/41200/2007) and João Loureiro (BPD/36601/2007) and the Spanish Ministerio de Educación y Ciencia financed the work of Victoria Ferrero (AP-2004-6394). This study was also partially financed under Grants PGIDT04PXIC31003PN from the Xunta de Galicia, CGL2006-13847-CO2-02 from the Spanish Dirección General de Investigación, Ciencia y Técnología and FEDER funds from the European Union to Luis Navarro.

Author information

Authors and Affiliations

  1. Centre for Functional Ecology and Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Calçada Martins de Freitas, 3001-455, Coimbra, Portugal

    Sílvia Castro & João Loureiro

  2. Department of Plant Biology and Soil Sciences, Faculty of Biology, University of Vigo, As Lagoas-Marcosende, 36310, Vigo, Spain

    Victoria Ferrero & Luis Navarro

  3. Animal Biodiversity Group, Department of Animal Biology, Plant Biology and Ecology, and CREAF, Autonomous University of Barcelona, E-08193, Bellaterra, Spain

    Xavier Espadaler

  4. CESAM and Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Paulo Silveira

Authors
  1. Sílvia Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Victoria Ferrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. João Loureiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xavier Espadaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luis Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sílvia Castro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castro, S., Ferrero, V., Loureiro, J. et al. Dispersal mechanisms of the narrow endemic Polygala vayredae: dispersal syndromes and spatio-temporal variations in ant dispersal assemblages. Plant Ecol 207, 359–372 (2010). https://doi.org/10.1007/s11258-009-9679-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-009-9679-z

Keywords

Search

Navigation