Abstract
A wide range of ant-plant mutualistic associations are known to occur in terrestrial ecosystems. Although many species of plants recruit ants to obtain protection from herbivores, myrmecophily is rare, since only few plant species are known to be adapted for pollination predominantly by ants. The annual herb, Euphorbia hirta, is characterized by the ‘ant-pollination syndrome’ including traits such as unisexual flowers, inconspicuous cyathia clustered in globose cymes, inflorescence-associated tiny nectaries and short, semi-erect stem. In present study, we aimed to examine the pollination ecology of Euphorbia hirta and the role of ants in its pollination. Field and laboratory experiments conducted to understand the association between E. hirta plants and ants revealed that seven ant species (belonging to five genera and three subfamilies) visited E. hirta plants. The visitation patterns of ants revealed that in a single foraging trip the ants visited a number of plants indicating their potential role in cross-pollination. Field-based exclusion experiments revealed production of significantly higher number of fruits in E. hirta plants under open pollination treatment as compared to other treatments. Scanning electron microscopy revealed that the adherence of the pollen grains to the bristles located on ant mouth-parts was facilitated by the three vertical, semi-circular grooves present on the grain surface. The number of fruits produced per plant was higher in ant-included plants as compared to only winged insect-pollinated and only self-pollinated plants suggesting that the plant-visiting ants are successful pollination vectors of E. hirta and while promoting self-pollination also contribute towards cross-pollination services.
Similar content being viewed by others
Data availability
The data are available in the body of the article.
References
Albuquerque AA, de Lima HA, Gonçalves-Esteves V, Benevides CR, Rodarte AT (2013) Myrsine parvifolia (Primulaceae) in sandy coastal plains marginal to Atlantic rainforest: a case of pollination by wind or by both wind and insects? Rev Bras Bot 36:65–73. https://doi.org/10.1007/s40415-013-0007-4
Aluri RJ (1990) Studies on pollination ecology in India: a review. Proc Ind Natl Sci Acad B 56:375–388
Aranda-Rickert A, Torréns J, Yela NI, Brizuela MM, Di Stilio VS (2021) Distance dependent contribution of ants to pollination but not defense in a dioecious, ambophilous gymnosperm. Front Plant Sci 2021:1979. https://doi.org/10.3389/fpls.2021.722405
Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. Am J Bot 71:421–426. https://doi.org/10.1002/j.1537-2197.1984.tb12527.x
Beattie AJ, Turnbull C, Hough T, Jobson S, Knox RB (1985) The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. Am J Bot 72:606–614. https://doi.org/10.1002/j.1537-2197.1985.tb08315.x
Berry PE, Calvo RN (1989) Wind pollination, self-incompatibility, and altitudinal shifts in pollination systems in the high Andean genus Espeletia (Asteraceae). Am J Bot 76:1602–1614. https://doi.org/10.1002/j.1537-2197.1989.tb15145.x
Byk J, Del-Claro K (2010) Nectar-and pollen-gathering Cephalotes ants provide no protection against herbivory: a new manipulative experiment to test ant protective capabilities. Acta Ethol 13:33–38
Cembrowski AR, Tan MG, Thomson JD, Frederickson ME (2014) Ants and ant scent reduce bumblebee pollination of artificial flowers. Am Nat 183:133–139
Chandra PH, Ramana KV, Krishna JR, Rani DS, Rao SP, Raju AS (2013) A study on interactions of insects with herbaceous plants in Visakhapatnam. In Advances in Pollen Spore Research. Today & Tomorrow’s Printers and Publishers: New Delhi, pp 69–79.
Claessens J, Seifert B (2017) Significant ant pollination in two orchid species in the Alps as adaptation to the climate of the alpine zone. Tuexenia 37:363–374. https://doi.org/10.14471/2017.37.005
Czechowski W, Markó B, Erős K, Csata E (2011) Pollenivory in ants (Hymenoptera: Formicidae) seems to be much more common than it was thought. Annales Zoologici 61:519–525. https://doi.org/10.3161/000345411X603364
de Vega C, Arista M, Ortiz PL, Herrera CM, Talavera S (2009) The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite. Ann Bot 103:1065–1075. https://doi.org/10.1093/aob/mcp049
de Vega C, Herrera CM, Dötterl S (2014) Floral volatiles play a key role in specialized ant pollination. Perspect Plant Ecol Evol Syst 16:32–42. https://doi.org/10.1016/j.ppees.2013.11.002
Del-Claro K, Rodriguez-Morales D, Calixto ES, Martins AS, Torezan-Silingardi HM (2019) Ant pollination of Paepalanthus lundii (Eriocaulaceae) in Brazilian savanna. Ann Bot 123:1159–1165. https://doi.org/10.1093/aob/mcz021
Delnevo N, van Etten EJ, Clemente N, Fogu L, Pavarani E, Byrne M, Stock WD (2020) Pollen adaptation to ant pollination: a case study from the Proteaceae. Ann Bot 126:377–386. https://doi.org/10.1093/aob/mcaa058
Dutton EM, Frederickson ME (2012) Why ant pollination is rare: new evidence and implications of the antibiotic hypothesis. Arthropod Plant Interact 6:561–569. https://doi.org/10.1007/s11829-012-9201-8
Ehrenfeld JG (1979) Pollination of three species of Euphorbia subgenus Chamaesyce, with special reference to bees. Am Midl Nat 1:87–98. https://doi.org/10.2307/2424904
Ekka PA, Rastogi N (2019) A single lycaenid caterpillar gets an ant-constructed shelter and uninterrupted ant attendance. Entomol Exp Appl 167:1012–1019. https://doi.org/10.1111/eea.12859
Ekpo OE, Pretorius E (2007) Asthma, Euphorbia hirta and its anti-inflammatory properties: news & views. S Afr J Sci 103:201–203
Faegri K, Van Der Pijl L (2013) Principles of pollination ecology. Pergamon Press
Gómez JM, Zamora R (1992) Pollination by ants: consequences of the quantitative effects on a mutualistic system. Oecologia 91:410–418
Gómez JM, Zamora R, Hódar JA, García D (1996) Experimental study of pollination by ants in Mediterranean high mountain and arid habitats. Oecologia 105:236–242. https://doi.org/10.1007/BF00328552
Haber WA, Frankie GW, Baker HG, Baker I, Koptur S (1981) Ants like flower nectar. Biotropica 13:211–214
Hickman JC (1974) Pollination by ants: a low-energy system. Science 184:1290–1292. https://doi.org/10.1126/science.184.4143.1290
Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin
Huang L, Chen S, Yang M (2012) Euphorbia hirta (Feiyangcao): a review on its ethnopharmacology, phytochemistry and pharmacology. J Med Plant Res 6:5176–5185. https://doi.org/10.5897/JMPR12.206
Ibarra-Isassi J, Sendoya SF (2016) Ants as floral visitors of Blutaparon portulacoides (A. St-Hil.) Mears (Amaranthaceae): an ant pollination system in the Atlantic Rainforest. Arthropod-Plant Interact 10:221–227. https://doi.org/10.1007/s11829-016-9429-9
Kumari S, Rastogi N (2018) Can a common and abundant plant-visiting ant species serve as a model for nine sympatric ant-mimicking arthropod species? Curr Sci 114:2189–2192
Kuriakose G, Sinu PA, Shivanna KR (2018) Ant pollination of Syzygium occidentale, an endemic tree species of tropical rain forests of the Western Ghats, India. Arthropod-Plant Interact 12:647–655. https://doi.org/10.1007/s11829-018-9613-1
Lach L (2005) Interference and exploitation competition of three nectar-thieving invasive ant species. Insectes Soc 52:257–262. https://doi.org/10.1007/s00040-005-0807-z
Luo CW, Li K, Chen XM, Huang ZY (2012) Ants contribute significantly to the pollination of a biodiesel plant, Jatropha curcas. Environ Entomol 41:1163–1168. https://doi.org/10.1603/EN12042
Martins DJ (2010) Pollination and seed dispersal in the endangered succulent Euphorbia brevitorta. J East Afr Nat Hist 99:9–17. https://doi.org/10.2982/028.099.0104
Martins C, Oliveira R, Aguiar L, Antonini Y (2020) Pollination biology of the endangered columnar cactus Cipocereus crassisepalus: a case of close relationship between plant and pollinator. Acta Bot Brasilica 34:177–184. https://doi.org/10.1590/0102-33062019abb0219
Merrill ED (1981) Plant life of the pacific world. C.E. Tuttle Co., Washington, Rutland
Narbona E, Ortiz PL, Arista M (2011) Linking self-incompatibility, dichogamy, and flowering synchrony in two Euphorbia species: alternative mechanisms for avoiding self-fertilization? PLoS ONE 6:e20668. https://doi.org/10.1371/journal.pone.0020668
Newstrom L, Robertson A (2005) Progress in understanding pollination systems in New Zealand. N Z J Bot 43:1–59. https://doi.org/10.1080/0028825X.2005.9512943
Ollerton J (1996) Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant–pollinator systems. J Ecol 84:767–769
Papp N (2004) Nectar and nectary studies on seven Euphorbia species. Acta Bot Hung 46:225–234. https://doi.org/10.1556/abot.46.2004.1-2.16
Rahman AH, Akter M (2013) Taxonomy and medicinal uses of Euphorbiaceae (Spurge) family of Rajshahi, Bangladesh. Res Plant Sci 1:74–80. https://doi.org/10.12691/plant-1-3-5
Raju AS, Ezradanam V (2002) Pollination ecology and fruiting behaviour in a monoecious species, Jatropha curcas L. (Euphorbiaceae). Curr Sci 10:1395–1398
Raju AS, Ramana KV (2018) Pollination ecology of Rhynchosia heynei Wight and Arn. (Leguminosae), an endemic medicinal herbaceous shrub species of peninsular India. J Inst Sci Tech 22:32–44. https://doi.org/10.3126/jist.v22i2.19592
Rastogi N (2007) Seasonal pattern in the territorial dynamics of the arboreal ant Oecophylla smaragdina (Hymenoptera: Formicidae). J Bombay Nat Hist Soc 104:13–17
Regupathy A, Ayyasamy R (2011) Ants in biofuel, Jatropha ecosystem: pollination and phoresy. Hexapoda 18:168–175
Samra S, Samocha Y, Eisikowitch D, Vaknin Y (2014) Can ants equal honeybees as effective pollinators of the energy crop Jatropha curcas L. under Mediterranean conditions? Gcb Bioenergy 6:756–767. https://doi.org/10.1111/gcbb.12105
Schürch S, Pfunder M, Roy BA (2000) Effects of ants on the reproductive success of Euphorbia cyparissias and associated pathogenic rust fungi. Oikos 88:6–12. https://doi.org/10.1034/j.1600-0706.2000.880102.x
Shukla RK, Singh H, Rastogi N (2016) How effective are disturbance–tolerant, agroecosystem–nesting ant species in improving soil fertility and crop yield? Appl Soil Ecol 108:156–164. https://doi.org/10.1016/j.apsoil.2016.08.013
Sinu PA, Sibisha VC, Reshmi MN, Reshmi KS, Jasna TV, Aswathi K, Megha PP (2017) Invasive ant (Anoplolepis gracilipes) disrupts pollination in pumpkin. Biol Invasions 19:2599–25607. https://doi.org/10.1007/s10530-017-1470-9
Srivastava AK (2001) Some studies on the climate of Varanasi. M.Sc. project work. Department of Geophysics, Banaras Hindu University
Unni AP, Mir SH, Rajesh TP, Ballullaya UP, Jose T, Sinu PA (2021) Native and invasive ants affect floral visits of pollinating honey bees in pumpkin flowers (Cucurbita maxima). Sci Rep 11:1–7. https://doi.org/10.1038/s41598-021-83902-w
Urbani CB, De Andrade ML (1997) Pollen eating, storing, and spitting by ants. Naturwissenschaften 84:256–258
Vanitha K, Bhat PS, Raviprasad TN, Srikumar KK (2017) Species composition of ants in cashew plantations and their interrelationships with cashew. Proc Natl Acad Sci India Sect B-Biol Sci 87:399–409. https://doi.org/10.1007/s40011-015-0600-3
Villamil N, Boege K, Stone GN (2018) Ant-pollinator conflict results in pollinator deterrence but no nectar trade-offs. Front Plant Sci 9:1093. https://doi.org/10.3389/fpls.2018.01093
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. https://doi.org/10.2307/2265575
Wyatt R (1981) Ant-pollination of the granite outcrop endemic Diamorpha smallii (Crassulaceae). Am J Bot 68:1212–1217. https://doi.org/10.1002/j.1537-2197.1981.tb07827.x
Yamasaki E, Sakai S (2013) Wind and insect pollination (ambophily) of Mallotus spp. (Euphorbiaceae) in tropical and temperate forests. Aust J Bot 61:60–66. https://doi.org/10.1071/BT12202
Acknowledgements
We are grateful to Prof. N.K. Dubey for kindly permitting the field studies in the Botanical Garden of Banaras Hindu University. We also thank DST-FIST for the infrastructural facility and to Prof. Chalapati Rao, Department of Geology, BHU for providing Scanning Electron microscopy (SEM) facility.
Funding
Not Applicable.
Author information
Authors and Affiliations
Contributions
JNS has contributed by conducting the field studies and by writing the article. NR made the contribution by proposing the hypothesis, designing the study and made appropriate corrections in the article.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Handling Editor: Isabel Alves dos Santos.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Samuel, J.N., Rastogi, N. Ants as pollination vectors of ant-adapted Euphorbia hirta L. plants. Arthropod-Plant Interactions 16, 361–372 (2022). https://doi.org/10.1007/s11829-022-09903-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-022-09903-2