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Are subordinate ants the best seed dispersers? Linking dominance hierarchies and seed dispersal ability in myrmecochory interactions

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Abstract

True myrmecochory involves the dispersal of elaiosome-bearing seeds by ants. Between the guild of ants that are attracted to these seeds, only a few of them will act as effective dispersers, that is, transporting the seeds to suitable sites (the nests) for germination and plant establishment. Ant communities are known to be highly hierarchical, and subordinate ants quickly deliver resources to their nest rather than consuming it on-site, thereby avoiding encounters with more dominant species. As a result of a series of studies that were carried out during summer in semi-arid Northwest Argentina, we have found that the most important seed disperser of the myrmecochorous plant Jatropha excisa Griseb. (Euphorbiaceae), the ant Pogonomyrmex cunicularius pencosensis Forel, was the most subordinate species during interspecific interactions. The daily timing of release of the J. excisa seeds through ballistic dispersal increased their probability of being removed by the highly thermophilic P. cunicularius pencosensis. Foraging during the warmest hours of the day allowed P. cunicularius pencosensis ants to avoid the risk of interference competition with dominant species, which also behaved as elaiosome predators. As a conclusion, subordinance behaviour appears to be integral to successful myrmecochory, and also the timing of seed release plays a key role in shaping the dynamics of myrmecochorous interactions. Therefore, ant-dispersed plants should not only favour their discovery by subordinate ants, but also should present their seeds at those times of the day when the behaviourally dominant ants are less active.

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References

  • Abraham E, del Valle HF, Roig F, Torres L, Coronato F, Godagnone R (2009) Overview of the geography of the Monte Desert biome (Argentina). J Arid Environ 73:144–153

    Article  Google Scholar 

  • Albrecht M, Gotelli N (2001) Spatial and temporal niche partitioning in grassland ants. Oecologia 126:134–141

    Article  Google Scholar 

  • Andersen AN (1995) A classification of Australian ant communities, based on functional groups which parallels plant life-forms in relation to stress and disturbance. J Biogeogr 22:15–29

    Article  Google Scholar 

  • Andersen AN (1997) Functional groups and patterns of organization in North American ant communities: a comparison with Australia. J Biogeogr 24:433–460

    Article  Google Scholar 

  • Aranda-Rickert A, Fracchia S (2010) Diplochory in two Jatropha (Euphorbiaceae) species of the Monte Desert of Argentina. Austral Ecol 35:226–235

    Article  Google Scholar 

  • Aranda-Rickert A, Fracchia S (2011) Pogonomyrmex cunicularius as the keystone disperser of the elaiosome-bearing Jatropha excisa seeds in semi-arid Argentina. Entomol Exp Appl 139:91–102

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Bernstein RA (1974) Seasonal food abundance and foraging activity in some desert ants. Am Nat 108:490–498

    Article  Google Scholar 

  • Bestelmeyer BT (2000) The trade-off between thermal tolerance and behavioural dominance in a subtropical South American ant community. J Anim Ecol 69:998–1009

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  PubMed  CAS  Google Scholar 

  • Calcaterra LA, Livore JP, Delgado A, Briano JA (2008) Ecological dominance of the red imported fire ant, Solenopsis invicta in its native range. Oecologia 156:411–421

    Article  PubMed  Google Scholar 

  • Cerdá X, Retana J, Cross S (1997) Thermal disruption of transitive hierarchies in Mediterranean ant communities. J Anim Ecol 66:363–374

    Article  Google Scholar 

  • Cerdá X, Retana J, Cross S (1998a) Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol 12:45–55

    Article  Google Scholar 

  • Cerdá X, Retana J, Manzaneda A (1998b) 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 

  • Cros S, Cerdá X, Retana J (1997) Spatial and temporal variations in the activity patterns of Mediterranean ant communities. ÉcoScience 4:269–278

    Google Scholar 

  • Cuezzo F, Claver S (2009) Two new species of the ant genus Pogonomyrmex (Hymenoptera: Formicidae) from Argentina. Rev Soc Entomol Arg 68:97–106

    Google Scholar 

  • Cushman JH, Beattie AJ (1991) Mutualisms-assessing the benefits to hosts and visitors. Trends Ecol Evol 6:193–195

    Article  PubMed  CAS  Google Scholar 

  • Davidson DW (1998) Resource discovery versus resource domination in ants: a functional mechanism for breaking the trade-off. Ecol Ent 23:484–490

    Article  Google Scholar 

  • Espadaler X, Gómez C (1996) Seed production, predation and dispersal in the Mediterranean myrmecochore Euphorbia characias (Euphorbiaceae). Ecography 19:7–15

    Article  Google Scholar 

  • Fellers JH (1987) Interference and exploitation in a guild of woodland ants. Ecology 68:1466–1478

    Article  Google Scholar 

  • Fellers JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78:69–76

    Article  Google Scholar 

  • Fernández F (2003) Introducción a las Hormigas de la Región Neotropical. Instituto Humboldt, Bogotá, Colombia

    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 

  • Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proc Natl Acad Sci USA 92:2994–2998

    Article  PubMed  CAS  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 

  • Giliberto J, Gutiérrez JR, Hajek ER (1980) Temperature effect on autochory in Colliguaya odorifera (Euphorbiaceae). Int J Biometeorol 24:199–202

    Article  Google Scholar 

  • Gove AD, Majer JD, Dunn RR (2007) A keystone ant species promotes seed dispersal in a “diffuse” mutualism. Oecologia 153:687–697

    Article  PubMed  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 

  • Hanzawa FM, Beattie AJ, Culver DC (1988) Directed dispersal: demographic analysis of an ant-seed mutualism. Am Nat 131:1–13

    Article  Google Scholar 

  • Heithaus ER, Humes M (2003) Variation in communities of seed-dispersing ants in habitats with different disturbance in Know County, Ohio. Ohio J Sci 103:89–97

    Google Scholar 

  • Herrera C (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Cambridge, MA

    Google Scholar 

  • Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511

    Article  Google Scholar 

  • Kusnezov N (1963) Zoogeografía de las hormigas en Sudamérica. Acta Zool Lill 19:25–186

    Google Scholar 

  • Kusnezov N (1978) Hormigas Argentinas. Clave para su Identificación. Miscelánea 61. Fundación Miguel Lillo, Tucumán, Argentina

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lourteig A, O’Donnell CA (1943) Euphorbiaceae Argentinae. Lilloa IX:77–143

  • Manzaneda AJ, Rey PJ (2009) Assessing ecological specialization of an ant-seed dispersal mutualism through a wide geographic range. Ecology 90:3009–3022

    Article  PubMed  Google Scholar 

  • Marshall DL, Beattie AJ, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant-seed interaction. J Chem Ecol 5:335–344

    Article  CAS  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, 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ohkawara K, Higashi S, Ohara M (1996) Effects of ants, ground beetles and seed-fall patterns on the myrmecochory of Erythronium japonicum Decne. (Liliaceae-Tulipaeae). Oecologia 106:500–506

    Article  Google Scholar 

  • Ohkawara K, Ohara M, Higashi S (1997) The evolution of ant-dispersal in a spring-ephemeral Corydalis ambigua (Papaveraceae): timing of seed-fall and effects of ants and ground beetles. Ecography 20:217–223

    Article  Google Scholar 

  • R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    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 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago

    Google Scholar 

  • Savolainen R, Vepsäläinen K (1988) A competition hierarchy among boreal ants: impact on resource partitioning and community structure. Oikos 51:135–155

    Article  Google Scholar 

  • Thompson JN (1981) Elaiosomes and fleshy fruits: phenology and selection pressures for ant-dispersed seeds. Am Nat 117:104–108

    Article  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago

    Google Scholar 

  • Turnbull CL, Culver DC (1983) The timing of seed dispersal in Viola nuttallii: attraction of dispersers and avoidance of predators. Oecologia 59:360–365

    Article  Google Scholar 

  • Vepsäläinen K, Savolainen R (1990) The effect of interference by formicine ants on the foraging of Myrmica. J Anim Ecol 59:643–654

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press, Cambridge, MA

    Google Scholar 

Download references

Acknowledgments

This study is part of the Ph.D. dissertation of A. A. R. at the Universidad de Buenos Aires, Argentina, which was financially supported by a Consejo Nacional de Investigaciones Científicas y Tecnológicas Grant. Field work was assisted by Lucía Krapovickas and Félix Fracchia. We thank Robert Johnson for gently providing the key for the identification of the P. cunicularius subspecies, and the two anonymous reviewers for their helpful manuscript suggestions.

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Correspondence to Adriana Aranda-Rickert.

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Aranda-Rickert, A., Fracchia, S. Are subordinate ants the best seed dispersers? Linking dominance hierarchies and seed dispersal ability in myrmecochory interactions. Arthropod-Plant Interactions 6, 297–306 (2012). https://doi.org/10.1007/s11829-011-9166-z

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  • DOI: https://doi.org/10.1007/s11829-011-9166-z

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