Abstract
To understand how food resource use and partitioning by closely related species allows local coexistence, it is key to determine whether a species’ diet reflects food availability or food preferences. Here, we analysed the diets, seed selection, and seed preferences of three closely related harvester ants: Messor barbarus, M. bouvieri, and M. capitatus. Sympatric within a Mediterranean shrubland, these species differ in foraging behaviour and worker polymorphism. For 2 years, we studied the ants’ diets and seed selection patterns as well as the local availability of seeds. Additionally, we performed a seed-choice experiment using a paired comparison design, offering the ants seeds from eight native plant species. The three ant species had the same general diet, which was primarily granivorous. Although they all consumed a wide variety of seeds, they mostly selected seeds from a small subset of plant species. Despite their morphological and behavioural differences, the ants displayed similar seed preferences that were highly consistent with their diets and seed selection patterns. Our results support the idea that the trophic ecology of these three harvester ants is driven by similar seed preferences rather than by their morphological and behavioural differences. Seed diversity and abundance were high near the ants’ nests, suggesting that seed availability is not limiting and could in fact favour local species coexistence.
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References
Andersen AN (1988) Immediate and longer-term effects of fire on seed predation by ants in sclerophyllous vegetation in south-eastern Australia. Aust J Ecol 13:285–293. https://doi.org/10.1111/J.1442-9993.1988.TB00976.X
Appleby MC (1983) The probability of linearity in hierarchies. Anim Behav 31:600–608. https://doi.org/10.1016/S0003-3472(83)80084-0
Arnan X, Rodrigo A, Retana J (2006) Post-fire recovery of Mediterranean ground ant communities follows vegetation and dryness gradients. J Biogeogr 33:1246–1258. https://doi.org/10.1111/J.1365-2699.2006.01506.X
Arnan X, Retana J, Rodrigo A, Cerdá X (2010a) Foraging behaviour of harvesting ants determines seed removal and dispersal. Insectes Soc 57:421–430. https://doi.org/10.1007/S00040-010-0100-7
Arnan X, Rodrigo A, Molowny-Horas R, Retana J (2010b) Ant-mediated expansion of an obligate seeder species during the first years after fire. Plant Biol 12:842–852. https://doi.org/10.1111/J.1438-8677.2009.00294.X
Arnan X, Ferrandiz-Rovira M, Pladevall C, Rodrigo A (2011) Worker size-related task partitioning in the foraging strategy of a seed-harvesting ant species. Behav Ecol Sociobiol 65:1881–1890. https://doi.org/10.1007/S00265-011-1197-Z
Arnan X, Molowny-Horas R, Rodrigo A, Retana J (2012) Uncoupling the effects of seed predation and seed dispersal by granivorous ants on plant population dynamics. PLoS ONE 7(8):e42869. https://doi.org/10.1371/JOURNAL.PONE.0042869
Arnan X, Lázaro-González A, Beltran N, Rodrigo A, Pol R (2022) Thermal physiology, foraging pattern, and worker body size interact to influence coexistence in sympatric polymorphic harvester ants (Messor spp.). Behav Ecol Sociobiol 76:1–12. https://doi.org/10.1007/s00265-022-03186-6
Azcárate FM, Peco B (2006) Effects of seed predation by ants on Mediterranean grassland related to seed size. J Veg Sci 17:353–360. https://doi.org/10.1111/J.1654-1103.2006.TB02455.X
Azcárate FM, Arqueros L, Sánchez AM, Peco B (2005) Seed and fruit selection by harvester ants, Messor barbarus, in Mediterranean grassland and scrubland. Funct Ecol 19:273–283. https://doi.org/10.1111/J.0269-8463.2005.00956.X
Baroni-Urbani C, Nielsen MG (1990) Energetics and foraging behaviour of the European seed harvesting ant Messor capitatus: II. Do ants optimize their harvesting? Physiol Entomol 15:449–461. https://doi.org/10.1111/J.1365-3032.1990.TB00534.X
Bastida F, Talavera S, Ortiz PL, Arista M (2009) The interaction between Cistaceae and a highly specific seed-harvester ant in a Mediterranean scrubland. Plant Biol 11:46–56. https://doi.org/10.1111/J.1438-8677.2008.00066.X
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. https://doi.org/10.1111/J.0021-8790.2004.00861.X
Behmer ST (2008) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187. https://doi.org/10.1146/annurev.ento.54.110807.090537
Bernard F (1983) Les fourmis et leur milieu en France méditerranéenne. Editions Lechevalier, Paris
Boyd R, Silk JB (1983) A method for assigning cardinal dominance ranks. Anim Behav 31:45–58. https://doi.org/10.1016/S0003-3472(83)80172-9
Cerdá X, Retana J (1994) Food exploitation patterns of two sympatric seed-harvesting ants Messor bouvieri (Bond.) and Messor capitatus (Latr.) (Hym., Formicidae) from Spain. J Appl Entomol 117:268–277. https://doi.org/10.1111/J.1439-0418.1994.TB00735.X
Cueto VR, Marone L, Lopez de Casenave J (2006) Seed preferences in sparrow species of the Monte desert, Argentina: implications for seed-granivore interactions. Auk 123:358–367. https://doi.org/10.1093/auk/123.2.358
Davidson DW (1977) Foraging ecology and community organization in desert seed-eating ants. Ecology 58:725–737. https://doi.org/10.2307/1936209
de Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843. https://doi.org/10.1006/ANBE.1997.0708
de Vries H, Stevens JMG, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592. https://doi.org/10.1016/J.ANBEHAV.2005.05.015
Detrain C, Pasteels J (2000) Seed preferences of the harvester ant Messor barbarus in a Mediterranean mosaic grassland (Hymenoptera: Formicidae). Sociobiol 35:35–48
Detrain C, Tasse O, Versaen M, Pasteels JM (2000) A field assessment of optimal foraging in ants: trail patterns and seed retrieval by the European harvester ant Messor barbarus. Insectes Soc 47:56–62. https://doi.org/10.1007/S000400050009
Devenish AJM, Gomez C, Bridle JR, Newton RJ, Sumner S (2019) Invasive ants take and squander native seeds: implications for native plant communities. Biol Invasions 21:451–466. https://doi.org/10.1007/S10530-018-1829-6/FIGURES/5
Elias M, Fontaine C, Frank van Veen FJ (2013) Evolutionary history and ecological processes shape a local multilevel antagonistic network. Curr Biol 23:1355–1359. https://doi.org/10.1016/j.cub.2013.05.066
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
Forister ML, Novotny V, Panorska AK, Baje L, Basset Y, Butterill PT, Cizek L, Coley PD, Dem F, Diniz IR, Drozd P, Fox M, Glassmire AE, Hazen R, Hrcek J, Jahner JP, Kaman O, Kozubowski TJ, Kursar TA, Dyer LA (2015) The global distribution of diet breadth in insect herbivores. Proc Natl Acad Sci USA 112:442–447. https://doi.org/10.1073/pnas.1423042112
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks, CA
Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061. https://doi.org/10.1073/pnas.0904106106
Grasso DA, Mori A, Le Moli F (1998) Chemical communication during foraging in the harvesting ant Messor capitatus (Hymenoptera, Formicidae). Insectes Soc 45:85–96. https://doi.org/10.1007/s000400050071
Heredia A, Detrain C (2005) Influence of seed size and seed nature on recruitment in the polymorphic harvester ant Messor barbarus. Behav Process 70:289–300. https://doi.org/10.1016/j.beproc.2005.08.001
Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci USA 105:4792–4795. https://doi.org/10.1073/pnas.0711998105
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Hulme PE (1997) Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111:91–98. https://doi.org/10.1007/s004420050212
Hulme PE, Benkman C (2002) Granivory. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Science, Oxford
Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994. https://doi.org/10.1111/j.1461-0248.2007.01093.x
Kaspari M (1996) Worker size and seed size selection by harvester ants in a neotropical forest. Oecologia 105:397–404. https://doi.org/10.1007/BF00328743
Kuřavová K, Sipos J, Wahab RA, Kahar RS, Kocarek P (2017) Feeding patterns in tropical groundhoppers (Tetrigidae): a case of phylogenetic dietary conservatism in a basal group of Caelifera. Zool J Linn Soc 179:291–302. https://doi.org/10.1111/zoj.12474
Kurushima H, Yoshimura J, Kim JK, Kim JK, Nishimoto Y, Sayama K, Kato M, Watanabe K, Hasegawa E, Roff DA, Shimizu A (2016) Co-occurrence of ecologically equivalent cryptic species of spider wasps. R Soc Open Sci 3:160119. https://doi.org/10.1098/rsos.160119
Landau HG (1951) On dominance relations and the structure of animal societies: I. Effect of inherent characteristics. Bull Math Biophys 13:1–19. https://doi.org/10.1007/BF02478336
Lassau SA, Hochuli DF (2004) Effects of habitat complexity on ant assemblages. Ecography 27:157–164. https://doi.org/10.1111/j.0906-7590.2004.03675.x
Lebas C, Galkowski C, Blatrix R, Wegnez P (2016) Fourmis d’europe occidentale. Delachaux et Niestlé
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003. https://doi.org/10.1111/j.1461-0248.2008.01229.x
MacMahon JA, Mull JF, Crist TO (2000) Harvester ants (Pogonomyrmex spp.): their community and ecosystem influences. Annu Rev Ecol Evol Syst 31:265–291. https://doi.org/10.1146/annurev.ecolsys.31.1.265
Miretti MF, Lopez de Casenave J, Pol RG (2019) Stereotyped seed preferences of the harvester ant Pogonomyrmex mendozanus in the central Monte desert. Arthropod Plant Int 13:771–778. https://doi.org/10.1007/s11829-019-09696-x
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: community ecology package. R package version 2.5-4. https://cran.rproject.org/web/packages/vegan/. Accessed 9 May 2023
Penn HJ, Crist TO (2018) From dispersal to predation: a global synthesis of ant-seed interactions. Ecol Evol 8:9122–9138. https://doi.org/10.1002/ece3.4377
Pirk GI, Lopez de Casenave J (2011) Seed preferences of three harvester ants of the genus Pogonomyrmex (Hymenoptera: Formicidae) in the Monte Desert: are they reflected in the diet? Ann Entomol Soc Am 104:212–220. https://doi.org/10.1603/AN10093
Plowes NJR, Johnson RA, Hölldobler B (2013) Foraging behavior in the ant genus Messor (Hymenoptera: Formicidae: Myrmicinae). Myrmecol News 18:33–49
Pol RG, Vargas GA, Marone L (2017) Behavioural flexibility does not prevent numerical declines of harvester ants under intense livestock grazing. Ecol Entomol 42:283–293. https://doi.org/10.1111/een.12388
Pol RG, Miretti F, Marone L (2022) Lower food intake due to domestic grazing reduces colony size and worsens the body condition of reproductive females of harvester ants. J Insect Conserv 26:583–592. https://doi.org/10.1007/s10841-022-00393-4
Price PW (2002) Resource-driven terrestrial interaction webs. Ecol Res 17:241–247. https://doi.org/10.1046/j.1440-1703.2002.00483.x
Pulliam HR, Brand MR (1975) The production and utilization of seeds in plains grassland of southeastern Arizona. Ecology 56:1158–1166. https://doi.org/10.2307/1936155
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Viena
Retana J, Cerdá X (1994) Worker size polymorphism conditioning size matching in two sympatric seed-harvesting ants. Oikos 71:261–266
Rodrigo A, Retana J (2006) Post-fire recovery of ant communities in Submediterranean Pinus nigra forests. Ecography 29:231–239. https://doi.org/10.1111/j.2006.0906-7590.04272.x
Schoener TW (1974) Resource partitioning in ecological communities: research on how similar species divide resources helps reveal the natural regulation of species diversity. Science 185:27–39. https://doi.org/10.1126/science.185.4145.27
Segev U, Tielbörger K, Lubin Y, Kigel J (2021) Ant foraging strategies vary along a natural resource gradient. Oikos 130:66–78. https://doi.org/10.1111/oik.07688
Solida L, Luiselli L, D’Angeli D, Testi A, Fanfani A (2014) Seed selection and coexistence in two sympatric Messor harvester ant species (Hymenoptera: Formicidae). Ital J Zool 82:1–7. https://doi.org/10.1080/11250003.2014.963177
Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Revi 86:640–657. https://doi.org/10.1111/j.1469-185X.2010.00164.x
Underwood EC, Christian CE (2009) Consequences of prescribed fire and grazing on grassland ant communities. Environm Entomol 38:325–332. https://doi.org/10.1603/022.038.0204
Valladares F, Bastias CC, Godoy O, Granda E, Escudero A (2015) Species coexistence in a changing world. Front Plant Sci 6:866. https://doi.org/10.3389/fpls.2015.00866
Whitford WG, Jackson E (2007) Seed harvester ants (Pogonomyrmex rugosus) as “pulse” predators. J Arid Environ 70:549–552. https://doi.org/10.1016/j.jaridenv.2007.01.005
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Ann Rev Ecol Evol Syst 36:519–539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431
Wilby A, Shachak M (2000) Harvester ant response to spatial and temporal heterogeneity in seed availability: pattern in the process of granivory. Oecologia 125:495–503. https://doi.org/10.1007/s004420000478
Willott SJ, Compton SG, Incoll LD (2000) Foraging, food selection and worker size in the seed harvesting ant Messor bouvieri. Oecologia 125:35–44. https://doi.org/10.1007/PL00008889
Wolff A, Debussche M (1999) Ants as seed dispersers in a mediterranean Old-field succession. Oikos 84:443–452. https://doi.org/10.2307/3546423
Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Prentice-Hall, Upper Saddle River
Acknowledgements
We thank Moisès Guardiola for helping with plant identification; Jessica Pearce-Duvet for editing the manuscript's English; and Florencia Miretti for helping with the seed-choice analysis.
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This work was supported by the Spanish Ministry of Science, Innovation, and Universities (grant number RYC-2015-18448 to XA).
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RGP and XA came up with the research; RGP, ALG, AR, and XA conducted the experiments, collected the data, and analysed the data; RGP wrote the manuscript with input from all the co-authors.
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Pol, R.G., Lázaro-González, A., Rodrigo, A. et al. Similar seed preferences explain trophic ecology of functionally distinct, but co-occurring and closely related harvester ants. Oecologia 203, 407–420 (2023). https://doi.org/10.1007/s00442-023-05475-x
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DOI: https://doi.org/10.1007/s00442-023-05475-x