Skip to main content
Log in

Lycaenid-tending ants can contribute to fitness gain of the infested host plants by providing nutrients

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Ground-nesting ant species are known to promote plant growth by soil nutrient enhancement. Camponotus compressus ants regularly visit the extrafloral nectary-bearing, lycaenid-infested cowpea, Vigna unguiculata plants and construct a shelter for the lycaenid caterpillars at the plant base. The present study shows that ants may influence the overall fitness of the infested cowpea plants by providing nutrients via soil and foliar pathways. Total carbon, nitrogen and phosphorous content of ant constructed shelter (ACS) soil of the lycaenid-harbouring plants were assessed, microbes from the ACS soil were isolated and their plant growth promotion ability was evaluated. Nitrate content of the ant faecal matter was estimated and overall plant fitness was assessed in terms of its growth and yield. The results revealed higher content of total C, N and P in the debris and chamber soil of ACS as compared to the control soil from the base of ant-excluded plants. The microbes isolated from the ACS and ant nest soil were found to possess plant growth promotion abilities. Ant faecal matter was found to contain substantial amount of nitrate. The ant-included, lycaenid-infested plants as well as those lacking the caterpillars demonstrated significantly higher number of pods, number of seeds per pod, root length, shoot length, plant height, number of leaves, plant fresh and dry weight as compared to the control plants. Lycaenid caterpillar tending ant species with a high propensity for visiting plants thus have the potential to increase plant fitness by increasing nutrient availability via multiple pathways.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agarwal VM, Rastogi N (2008) Deterrent effect of a guild of extrafloral nectary-visiting ant species on Raphidopalpa foveicollis, a major insect pest of sponge gourd, Luffa cylindrica. Entomol Exp Appl 128:303–311

    Google Scholar 

  • Agarwal VM, Rastogi N (2009) Food resource and temporal partitioning amongst a guild of predatory agroecosystem-inhabiting ant species. Curr Zool 55:366–375

    Google Scholar 

  • Agarwal VM, Rastogi N (2010) Ants as dominant insect visitors of the extrafloral nectaries of sponge gourd plant, Luffa cylindrical (L.) (Cucurbitaceae). Asian Myrmecol 3:45–54

    Google Scholar 

  • Akand S, Bashar MA, Khan HR (2015) Biology of gram blue butterfly, Euchrysops cnejus (Fabricius) (Lycaenidae: Lepidoptera) and its relationship with the phenology of host-plant (Vigna unguiculata: Fabaceae). J Bangladesh Acad Sci 39:241–248

    Google Scholar 

  • Allen SE, Grimshaw ΗΜ, Parkinson JA, Quarnby C (1974) Chemical analysis of ecological materials. Blackwell, Oxford, UK

    Google Scholar 

  • APHA/AWWA/WPCF (1998) Standard methods for the examination of water and wastewaters, American Public Health Association, American Water Works Association and Water Pollution Control Federation, 12th ed. Washington (DC), New York.

  • Bano N, Musarrat J (2003) Characterization of a new Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Curr Microbiol 46:0324–0328

    CAS  Google Scholar 

  • Bertoni G (2012) A nitrate transporter for both roots and shoots. Plant Cell 24:1

    CAS  PubMed  PubMed Central  Google Scholar 

  • Birkhofer K, Bezemer TM, Bloem J, Bonkowski M, Christensen S, Dubois D et al (2008) Long-term organic farming fosters below and aboveground biota: implications for soil quality, biological control and productivity. Soil Biol Biochem 40:2297–2308

    CAS  Google Scholar 

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Google Scholar 

  • Culliney TW (2013) Role of arthropods in maintaining soil fertility. Agriculture 3:629–659

    Google Scholar 

  • Dean WRJ, Yeaton RI (1993) The influence of harvester ant Messor capensis nest-mounds on the productivity and distribution of some plant species in the southern Karoo, South Africa. Vegetatio 106:21–35

    Google Scholar 

  • Detrain C, Fichaux M, Verheggen F (2017) Tuned protection of aphids by ants against a predatory hoverfly. Ecol Entomol 42:235–244

    Google Scholar 

  • Doan TT, Henry-des-Tureaux T, Rumpel C, Janeau JL, Jouquet P (2015) Impact of compost, vermicompost and biochar on soil fertility, maize yield and soil erosion in Northern Vietnam: a three year mesocosm experiment. Sci Total Environ 514:147–154

    CAS  PubMed  Google Scholar 

  • Ekka PA, Rastogi N (2019) A single lycaenid caterpillar gets an ant-constructed shelter and uninterrupted ant attendance. Entomol Exp appl 167:1–8

    Google Scholar 

  • Evans TA, Dawes TZ, Ward PR, Lo N (2011) Ants and termites increase crop yield in a dry climate. Nat Commun 2:262

    PubMed  PubMed Central  Google Scholar 

  • Fagundes R, Ribeiro SP, Del-Claro K (2013) Tending-ants increase survivorship and reproductive success of Calloconophora pugionata Drietch (Hemiptera, Membracidae), a trophobiont herbivore of Myrcia obovata O. Berg (Myrtales, Myrtaceae). Sociobiology 60:11–19

    Google Scholar 

  • Farina R, Beneduzia A, Ambrosinia A, de Campos SB, Lisboa BB, Wendisch V, Vargas LK, Passaglia LMP (2012) Diversity of plant growth-promoting rhizobacteria communities associated with the stages of canola growth. Appl Soil Ecol 55:44–52

    Google Scholar 

  • Fernández V, Brown PH (2013) From plant surface to plant metabolism: the uncertain fate of foliar-applied nutrients. Front Plant Sci 4:289

    PubMed  PubMed Central  Google Scholar 

  • Fiedler K (2001) Ants that associate with Lycaeninae butterfly larvae: diversity, ecology and biogeography. Divers Distrib 7:45–60

    Google Scholar 

  • Fiedler K (2012) The host genera of ant-parasitic Lycaenidae butterflies: a review. Psyche 2012:1–10

    Google Scholar 

  • Finer L, Jurgensen MF, Domisch T, Kilpelainen J, Neuvonen S, Punttila P, Risch AC, Ohashi M, Niemela P (2013) The role of wood ants (Formica rufa group) in carbon and nutrient dynamics of a boreal Norway spruce forest ecosystem. Ecosystems 16:196–208

    CAS  Google Scholar 

  • Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers Conserv 7:1221–1244

    Google Scholar 

  • Frouz J, Jilková V (2008) The effects of ants on soil properties and processes (Hymenoptera: Formicidae). Myrmecol News 11:191–199

    Google Scholar 

  • Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, De Ley J (1989) Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov.as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov. Int J Syst Bacteriol 39:337–345

    Google Scholar 

  • Gegenbauer C, Mayer VE, Zotz G, Richter A (2012) Uptake of ant-derived nitrogen in the myrmecophytic orchid Caularthon bilamellatum. Ann Bot 110:757–765

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grobelak A, Hiller J (2017) Bacterial siderophores promote plant growth: Screening of catechol and hydroxamate siderophores. Int J Phytoremediat 19:825–833

    CAS  Google Scholar 

  • Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Harvard

    Google Scholar 

  • Holmes B, Popoff M, Kiredjian M, Kersters K (1988) Ochrobactrum anthropi gen. nov., sp. nov. from human clinical specimens and previously known as group Vd. Int J Syst Bacteriol 38:406–416

    Google Scholar 

  • Jackson ML (1958) Soil Chemical Analysis. Prentice Hall Inc., Englewood, Cliffs, NJ, USA

    Google Scholar 

  • John P, Karmaly KA (2016) A study on the Diversity and Distribution of Genus Camponotus Mayr (Hymenoptera: Formicidae) in Kerela: Ecologically Significant Agents in Ecosystem Functioning. Arthropod Diversity and Conservation in the Tropics and Sub-tropics. Springer, Singapore, pp 255–270

    Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients in the rhizosphere. Plant Soil 166:247–257

    CAS  Google Scholar 

  • Jouquet P, Dauber J, Lagerlöf J, Lavelle P, Lepage M (2006) Soil invertebrates as ecosystem engineers: Intended and accidental effects on soil and feedback loops. Appl Soil Ecol 32:153–164

    Google Scholar 

  • Kilpeläinen J, Finér L, Niemelä P, Domisch T, Neuvonen S, Ohashi O, Risch AC, Sundström L (2007) Carbon, nitrogen and phosphorus dynamics of ant. Appl Soil Ecol 36:156–163

    Google Scholar 

  • Khan SR, Singh SK, Rastogi N (2017) Heavy metal accumulation and ecosystem engineering by two common mine site-nesting ant species: implications for pollution-level assessment and bioremediation of coal mine soil. Environ Monit Assess 189:195

    PubMed  Google Scholar 

  • Kulkarni GB, Nayak AS, Sajjan SS, Oblesha A, Karegoudar TB (2013) Indole-3-acetic acid biosynthetic pathway and aromatic amino acid amino transferase activities in Pantoea dispersa strain GPK. Lett Appl Microbiol 56:340–347

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Kumari S, Singh H, Rastogi N (2016) Influence of the sugar-loving ant, Camponotus compressus (Fabricus, 1787) on soil physico-chemical characteristics. Halteres 7:163–174

    Google Scholar 

  • Kuo J, pate JS, (1985) The extrafloral nectaries of cowpea (Vigna unguiculata (L.) Walp): I. Morphology, anatomy and fine structure. Planta 166:15–27

    CAS  PubMed  Google Scholar 

  • Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15

    Google Scholar 

  • Liao X, Lovett B, Fang W, Leger RJSt, (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163:980–991

    CAS  PubMed  Google Scholar 

  • Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56

    CAS  PubMed  Google Scholar 

  • Narendra A, Gibb H, Ali TM (2011) Structure of ant assemblages in Western Ghats, India: role of habitat, disturbance and introduced species. Insect Conserv Diver 4:132–141

    Google Scholar 

  • Nettimi RP, Iyer P (2015) Patch fidelity in Camponotus compressus ants foraging on honeydew secreted by treehoppers. Curr Sci 109:362–366

    Google Scholar 

  • Offenberg J (2007) The distribution of weaver ant pheromones on host trees. Insectes Soc 54:248–250

    Google Scholar 

  • Panwar M, Tewari R, Gulati A, Nayyar H (2016) Indigenous salt-tolerant rhizobacterium Pantoea dispersa (PSB3) reduces sodium uptake and mitigates the effects of salt stress on growth and yield of chickpea. Acta Physiol Plant 38:278

    Google Scholar 

  • Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annu Rev Entomol 47:733–771

    CAS  PubMed  Google Scholar 

  • Pinkalski C, Jensen KMV, Damgaard C, Offenberg J (2018) Foliar uptake of nitrogen from ant faecal droplets: An overlooked service to ant-plants. J Ecol 106:289–295

    CAS  Google Scholar 

  • Radzki W, Gutierrez Manero FJ, Algar E, Lucas Gracía JA, Gracía-Villaraco A, Ramos Solano B (2013) Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Leeuwenhoek 104:321–330

    CAS  PubMed  Google Scholar 

  • Rosumek FB, Silveira FAO et al (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549

    PubMed  Google Scholar 

  • Saini A, Nain L, Garg V, Saxena J (2017) Improvement of growth, yield, and pigmentation of mung bean plants using Ochrobactrum intermedium CP-2 as bioinoculant. Clean-Soil Air Water 45:1500670

    Google Scholar 

  • Sanders D, Van Veen FJF (2011) Ecosystem engineering and predation: the multi-trophic impact of two ant species. J Anim Ecol 80:569–576

    PubMed  Google Scholar 

  • Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta AD, Mishra PK, Gupta HS (2008) Characterization of a cold tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J Microbiol Biotechnol 24:955–960

    CAS  Google Scholar 

  • Shukla RK, Rastogi N, Singh H (2018) Contribution of the nutrient-enriched ant nest debris soil to growth and yield of kalmegh (Andrographis paniculata) under natural and experimental field conditions. Biol Agric Hortic 34:173–185

    Google Scholar 

  • 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

    Google Scholar 

  • Shukla RK, Singh H, Rastogi N, Agarwal VM (2013) Impact of abundant Pheidole ant species on soil nutrients in relation to the food biology of the species. Appl Soil Ecol 71:15–23

    Google Scholar 

  • Solano PJ, Dejean A (2004) Ant-fed plants: comparison between three geophytic myrmecophytes. Biol J Linnean Soc 83:433–443

    Google Scholar 

  • Stiegler JC, Richardson MD, Karcher DE (2011) Foliar nitrogen uptake following urea application to putting green turfgrass species. Crop Sci 51:1253–1260

    Google Scholar 

  • Toro ID, Ribbons RR, Pelini SL (2012) The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol News 17:133–146

    Google Scholar 

  • Treseder KK, Davidson DW, Ehleringer JR (1995) Absorption of ant-provided carbon dioxide and nitrogen by a tropical epiphyte. Nature 375:137–139

    CAS  Google Scholar 

  • Uscola M, Villar-Salvador P, Oliet J, Warren C (2014) Foliar absorption and root translocation of nitrogen from different chemical forms in seedlings of two Mediterranean trees. Environ Exp Bot 104:34–43

    CAS  Google Scholar 

  • Varshney RK (1997) Index Rhopalocera indica Part III. Genera of Butterflies from India and neighbouring countries (Lepidoptera : (C) Lycaenidae). Oriental Insects 31:88–138

    Google Scholar 

  • Varshney RK, Peter S (2015) A synoptic catalogue of the butterflies of India. New Delhi: Butterfly Research Centre, Bhimtal and Indivov Publishing, New Delhi. P 143.

  • Wagner D (1997) The influence of ant nests on Acacia seed production, soil chemistry, and herbivory. J Ecol 85:83–94

    Google Scholar 

  • Wagner D, Jones JB, Gordon DM (2004) Development of harvester ant colonies alters soil chemistry. Soil Biol Biochem 36:797–804

    CAS  Google Scholar 

  • Wagner D, Nicklen EF (2010) Ant nest location, soil nutrients and nutrient uptake by ant-associated plants: does extrafloral nectar attract ant nests and thereby enhance plant nutrition? J Ecol 98:614–624

    Google Scholar 

  • Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils: Effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264

    CAS  Google Scholar 

  • Wilson EO (1976) Which are the most prevalent ant genera? Studia Entomologica 19:187–200

    Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu S, Liu Y, Wang J, Yin T, Han Y, Wang X, Huang Z (2015) Isolation and potential of Ochrobactrum sp. NW-3 to increase the growth of cucumber. IJAPR 3:341–350

    Google Scholar 

Download references

Acknowledgements

The authors thank the two anonymous reviewers for their constructive comments and suggestions. Funding support from Council of Scientific and Industrial Research (File No. : 09/013 (0536)/ 2014- EMR-I), New Delhi, India, is gratefully acknowledged. We are thankful to Prof. N.K. Dubey for kindly permitting the field studies in the botanical garden of Banaras Hindu University.

Author information

Authors and Affiliations

Authors

Contributions

Priya A. Ekka has contributed by conducting the field studies and experiments, and by writing the article. Neelkamal Rastogi made the contribution in designing the study and made appropriate corrections in the article. Hema Singh has contributed by extending the laboratory facilities for soil nutrient analysis and for assessing the plant growth parameters. Harikesh B. Singh has contributed by extending the laboratory facilities for study of microbes and their plant growth promotion ablates. Shatrupa Ray has made the contribution by helping in the isolation of microbes and in conducting microbe related experiments.

Corresponding author

Correspondence to Neelkamal Rastogi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Jouni Sorvari and Heikki Hokkanen.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendices

Appendix

Appendix 1

See Table 3.

Table 3 Plant growth promotion ability of the bacterial isolates from the four categories of soil collected from cowpea plant base

Appendix 2

See Table 4.

Table 4 Plant growth promotion ability of the bacterial isolates from Camponotus compressus main and satellite nest debris pile and chamber soil

Appendix 3

See Table 5.

Table 5 Growth parameters, i.e. root length, shoot length and plant height (cm), fresh and dry weight (g plant−1) of root, shoot, leaves and plants, number of branches, leaves and pods plant−1 and seeds pod−1 of ant-excluded, ant-included (lycaenid absent) and ant-included (lycaenid present) Vigna unguiculata plants

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ekka, P.A., Rastogi, N., Singh, H. et al. Lycaenid-tending ants can contribute to fitness gain of the infested host plants by providing nutrients. Arthropod-Plant Interactions 14, 745–757 (2020). https://doi.org/10.1007/s11829-020-09785-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-020-09785-2

Keywords

Navigation