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Elaiosome-bearing plants from the Iberian Peninsula and the Balearic Islands

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Abstract

The importance of many mutualistic interactions is poorly understood because information on their frequency and distribution at wide spatial scales is lacking. One such interaction is that between ants and plants bearing diaspores equipped with elaiosomes, which function as a reward for ants in exchange for dispersion. Our aim was to estimate the number of taxa having elaiosome-bearing diaspores in the Ibero-Balearic territory and its relationship to several factors. We estimated that at least 572 species and subspecies, almost one-third endemic, are present, which corresponds to ca. 5.1% of European angiosperms and 9% of Iberian ones. Because this number of elaiosome-bearing taxa is much higher than those given so far for the Northern Hemisphere, the Ibero-Balearic territory should be considered an important center of myrmecochory, with myrmecochorous species richness significantly positively correlated with ruggedness, latitude, and longitude. In contrast to other myrmecochorous territories (Australia and Cape Province), where numerous trees and shrubs develop on acid substrates, most myrmecochores in the Ibero-Balearic area are perennial herbs occupying basic substrates. Such perennial herbs are more frequent in the Eurosiberian floristic region, whereas annuals abound in the Mediterranean region. The enumerated taxa mainly inhabit forests, scrubs, and anthropized sites. Among them, 56.5% carry the elaiosome on seeds (especially strophiole and caruncle types). In 36.7%, the elaiosome is borne on indehiscent fruits, such as achenes in Asteraceae, where they are found either at the base of the style or the basal hilum, and at the base of nutlets (Boraginaceae and Lamiaceae).

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References

  • Aedo C, Medina L, Fernández-Albert M (2013) Species richness and endemicity in the Spanish vascular flora. Nord J Bot 30:1–11

    Google Scholar 

  • Aedo C, Buira A, Medina L, Fernández-Albert M (2017) The Iberian vascular Flora: richness, endemicity and distribution patterns. In: Loidi J (ed) The vegetation of the Iberian Peninsula, vol. 1, Plant and vegetation, vol 12. Springer International Publishing, Cham, pp 101–130

    Chapter  Google Scholar 

  • Affre L, Thompson JD, Debussche M (1995) The reproductive biology of the Mediterranean endemic Cyclamen balearicum Willk. (Primulaceae). Bot J Linn Soc 118:309–330

    Google Scholar 

  • 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 

  • APG IV (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  • Barroso A, Amor F, Cerdá X, Boulay RR (2013) Dispersal of non-myrmecochorous plants by a ‘“keystone disperser”’ ant in a Mediterranean habitat reveals asymmetric interdependence. Insect Soc 60:75–86

    Article  Google Scholar 

  • Bas JM, Oliveras J, Gómez C (2007) Final seed fate and seedling emergence in myrmecochorus plants: effects of ants and plant species. Sociobiology 50:101–111

    Google Scholar 

  • Beattie A (1983) Distribution of ant-dispersed plants. Sonderb Naturwiss Vereins Hamburg 7:249–270

    Google Scholar 

  • Beattie AJ, Culver DC (1981) The guild of myrmecochores in the herbaceous flora of West Virginia forest. Ecology 62:107–115

    Article  Google Scholar 

  • Beattie AJ, Hughes L (2002) Ant–plant interactions. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions. An evolutionary approach. Blackwell Science, Oxford, pp 211–235

    Google Scholar 

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

    Article  Google Scholar 

  • Boieiro M, Espadaler X, Gómez 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

    Article  Google Scholar 

  • Bond WJ, Slingsby P (1983) Seed dispersal by ants in shrublands of the Cape Province and its evolutionary implications. S Afr J Sci 79:231–233

    Google Scholar 

  • Bond WJ, Yeaton R, Stock WD (1991) Myrmecochory in Cape fynbos. In: Huxley CR, Cutler DF (eds) Ant–plant interactions. Oxford University Press, Oxford, pp 448–462

    Google Scholar 

  • Boulay BR, 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, Coll-Toledano J, Manzaneda AJ, Cerdá X (2007) Geographic variations in seed dispersal by ants: are plant and seed traits decisive? Naturwissenschaften 94:242–246

    Article  CAS  PubMed  Google Scholar 

  • Bresinsky A (1963) Bau, entwicklungsgeschichte und inhasltostoffe der elaiosomen. Studien zur myrmekochoren verbreitung von samen und früchten. Bibl Bot 126:1–54

    Google Scholar 

  • Bresinsky A, Körner C, Kadereit JW, Neuhaus H, Sonnewald U (2013) Strasburger’s plant sciences, including prokaryotes and Fungi, 36th edn. Springer, Berlin

    Book  Google Scholar 

  • Buira A, Aedo C, Medina L (2017) Spatial patterns of the Iberian and Balearic endemic vascular flora. Biodivers Conserv 26:479–508

    Article  Google Scholar 

  • Castroviejo S (coord) (1986–2020) Flora iberica. Real Jardín Botánico, CSIC, Madrid

  • Christenhusz MJM, Fay MF, Chase MW (2017) Plants of the world. An illustrated encyclopedia of vascular plants. Royal Botanic Gardens, Kew

    Book  Google Scholar 

  • Collins PM, Davis BAS, Kaplan JO (2012) The mid-Holocene vegetation of the Mediterranean region and southern Europe, and comparison with the present day. J Biogeogr 39:1848–1861

    Article  Google Scholar 

  • de Vega C, Arista M, Ortiz PL, Herrera CM, Talavera S (2011) Endozoochory by beetles: a novel seed dispersal mechanism. Ann Bot Lond 107:629–637

    Article  Google Scholar 

  • Delgado Santana F, Cazetta E, Delabie JHC (2013) Interactions between ants and non-myrmecochorous diaspores in a tropical wet forest in southern Bahia. Braz J Trop Ecol 29:71–80

    Article  Google Scholar 

  • Devesa JA, Quintanar A, García MA (eds) (2014) Compositae. Flora iberica 16(1). Real Jardín Botánico, CSIC, Madrid

  • 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 

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

    Article  Google Scholar 

  • Fischer RC, Oelzant 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

    Article  Google Scholar 

  • 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

    Article  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) Geografical 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 

  • Goerlich FJ, Cantarino I (2010) Rugosidad del terreno. Una característica del paisaje poco estudiada. Documentos de Trabajo 07/10. Ed Fundación BBVA, Bilbao

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

    Article  Google Scholar 

  • Gómez C, Espadaler X (2013) An update of the world survey of myrmecochorous dispersal distances. Ecography 36:1193–1201

    Article  Google Scholar 

  • Gómez C, Espadaler X, Bas JM (2005) Ant behaviour and seed morphology: a missing link of myrmecochory. Oecologia 146:244–246

    Article  PubMed  Google Scholar 

  • Gorb E, Gorb S (2003) Seed dispersal by ants in a deciduous forest ecosystem. Mechanisms, strategies, adaptations. Springer-Science+Business Media, BV, Dordrecht

    Book  Google Scholar 

  • Gordon SCC, Meadley-Dunphy SA, Prior KM, Frederickson ME (2019) Asynchrony between ant seed dispersal activity and fruit dehiscence of myrmecochorous plants. Am J Bot 106:71–80

    Article  PubMed  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 myrmecochorus plants an adaptation for ant dispersal? Plant Spec Biol 21:165–171

    Article  Google Scholar 

  • Leal IR, Leal LC, Andersen AN (2015) The benefits of myrmecochory: a matter of stature. Biotropica 47:281–285

    Article  Google Scholar 

  • Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2009) Ants sow the seeds of global diversification in flowering plants. PLoS One 4(5):35480

    Article  Google Scholar 

  • 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 12:43–55

    Article  Google Scholar 

  • Levine N, Ben-Zvi G, Seifan M, Giladi I (2019) Investment in reward by ant-dispersed plants consistently selects for better partners along a geographic gradient. AoB Plants 11(3):1–13

    Article  Google Scholar 

  • Lisci M, Bianchini M, Pacini E (1996) Structure and function of the elaiosome in some angiosperm species. Flora 191:131–141

    Article  Google Scholar 

  • Manzaneda AJ, Rey PJ (2008) Geographic variation in seed removal of a myrmecochorous herb: influence of variation in functional guild and species composition of the disperser assemblage through spatial and temporal scales. Ecography 31:583–591

    Article  Google Scholar 

  • 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 

  • Manzaneda AJ, Rey PJ, Alcántara JM (2009) Conflicting selection on diaspore traits limits the evolutionary potential of seed dispersal by ants. J Evol Biol 22:1407–1477

    Article  PubMed  Google Scholar 

  • Mayer V (2009) Tragedienste gegen nahrung: ameisen als frucht- und samenverbreiter. Denisia 25:107–118

    Google Scholar 

  • Mayer V, Ölzant S, Fischer RC (2005) Myrmecochorous seed dispersal in temperate regions. In: Forget P-M, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate: predation, and dispersal and seedling establishment. CABI Publishing, Wallingford, pp 175–195

    Chapter  Google Scholar 

  • Médail F, Quézel P (1999) Biodiversity hotspots in the Mediterranean Basin: setting global conservation priorities. Conserv Biol 13:1510–1513

    Article  Google Scholar 

  • Milewski AV, Bond WJ (1982) Convergence of myrmecochory in Mediterranean Australia and South Africa. In: Buckley RC (ed) Ant–plant interactions in Australia. Dr W Junk Publishers, The Hague, cap 9, pp 89–98

  • Miller ChN, Whitehead SR, Kwit Ch (2020) Effects of seed morphology and elaiosome chemical composition on attractiveness of five Trillium species to seed-dispersing ants. Ecol Evol 10:2860–2873

    Article  PubMed  PubMed Central  Google Scholar 

  • Montesinos D, Correia M, Castro S, French K, Rodríguez-Echeverría S (2018) Diminishing importance of elaiosomes for acacia seed removal in non-native ranges. Evol Ecol 32:601–621

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi H (1994) Myrmecochorus adaptations of Corydalis species (Papaveraceae) in southern Japan. Ecol Res 9:1–8

    Article  Google Scholar 

  • Oberrath R, Böhning-Gaese K (2002) Phenological adaptation 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  CAS  PubMed  Google Scholar 

  • Orians GH, Milewski AV (2007) Ecology of Australia: the effects of nutrient-poor soils and intense fires. Biol Rev 82:393–423

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pemberton RW, Irving DW (1990) Elaiosomes on weed seeds and the potential for myrmecochory in naturalized plants. Weed Sci 38:615–619

    Article  Google Scholar 

  • Pfeiffer M, Huttenlocher H, Ayasse M (2010) Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants. Funct Ecol 24:545–555

    Article  Google Scholar 

  • Rey PJ, Herrera CM, Guitián J, Cerdá X, Sánchez-Lafuente AM, Medrano M, Garrido JL (2006) The geographic mosaic in predispersal interactions and selection on Helleborus foetidus (Ranunculaceae). J Evol Biol 19:21–34

    Article  CAS  PubMed  Google Scholar 

  • Rivas Martínez S, Penas A, Díaz TE (2004) Worldwide bioclimatic classification system. Phytosociolocal Research Center. www.globalbioclimatics.org. Accessed 25 Nov 2020

  • Rodríguez-Riaño T, Valtueña FJ, Ortega-Olivencia A (2006) Megasporogenesis, megagametogenesis and ontogeny of the aril in Cytisus striatus and C. multiflorus (Leguminosae: Papilionoideae). Ann Bot Lond 98:777–791

    Article  Google Scholar 

  • Sernander R (1906) Entwurf einer Monographie der europäischen Myrmekochoren. Kungl Svenska Vetenskapsakad Handlingar 41:1–409

    Google Scholar 

  • Servigne P (2008) Étude expérimentale et comparative de la myrmécochorie: le cas des fourmis dispersatrices Lasius niger et Myrmica rubra. Thèse de Doctorat. Communauté française de Belgique, Université Libre de Bruxelles

  • Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. WH Freeman and Co, New York

    Google Scholar 

  • Turner KM, Frederickson ME (2013) Signals can trump rewards in attracting seed-dispersing ants. PLoS One 8(8):e71871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tutin TG et al (eds) (1964–1980) Flora europaea, 5 volumes. Cambridge University Press, Cambridge

  • Tutin TG et al (eds) (1993) Flora europaea, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161

    Article  PubMed  Google Scholar 

  • Vander Wall SB, Barga SC, Seaman AE (2017) The geographic distribution of seed-dispersal mutualisms in North America. Evol Ecol 31:725–740

    Article  Google Scholar 

  • Warren RJ, Giladi I (2014) Ant-mediated seed dispersal: a few ants species (Hymenoptera: Formicidae) benefit many plants. Myrmecol News 20:129–140

    Google Scholar 

  • Warren RJ, Giladi I, Bradford MA (2014) Competition as a mechanism structuring mutualisms. J Ecol 102:486–495

    Article  Google Scholar 

  • Wolff A, Debussche M (1999) Ants as seed dispersers in a Mediterranean old-field succession. Oikos 84:443–452

    Article  Google Scholar 

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Acknowledgements

This research was supported by the Economy and Infrastructure Council of Extremadura (Grant Number GR18034), co-financed by the European Regional Development Fund. We thank Miguel González (University of Extremadura) for his help in the statistical analyses, Juan A. Devesa (University of Córdoba) for providing us with information of interest, and Barbara Goodson from Edanz Group (www.edanzediting.com/ac) for editing the English text of a draft of this manuscript. We thank two anonymous reviewers—especially the one who invested considerable time on multiple reviews—for their important comments that greatly improved the manuscript.

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This research was supported by the Economy and Infrastructure Council of Extremadura (Grant Number GR18034), co-financed by the European Regional Development Fund.

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AOO was responsible for the conception and design of this study. Material preparation and data collection was done by AOO with the help of TRR, JL and FJV; statistical analyses and figures design were performed by TRR. The Appendix D, the study of the protection level of each taxon and the possible invasive species were carried out by JL. All the photos and the Mantel test were realized by FJV. AOO wrote the first draft of the manuscript, all authors commented and improved it. All read and approved the final manuscript.

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Correspondence to Ana Ortega-Olivencia.

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Ortega-Olivencia, A., Rodríguez-Riaño, T., López, J. et al. Elaiosome-bearing plants from the Iberian Peninsula and the Balearic Islands. Biodivers Conserv 30, 1137–1163 (2021). https://doi.org/10.1007/s10531-021-02137-3

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