Skip to main content

Advertisement

Log in

Natural history and ecology of fungus-farming ants: a field study in Atlantic rainforest

Insectes Sociaux Aims and scope Submit manuscript

Abstract

Ants in the subtribe Attina belong to a monophyletic group, exclusive to the New World, that contains approximately 250 described species. All attine ants have a mutualistic relationship with the fungus they cultivate as food source. The present study provides a natural history and ecological account of five species of fungus-farming ants in the Brazilian Atlantic rainforest: Mycocepurus smithii, Mycetarotes parallelus, Mycetophylax morschi, Sericomyrmex parvulus, and Sericomyrmex saussurei. Specifically, we investigated nesting and foraging behavior and daily activity rhythms, and identified the substrates collected for fungiculture. Nests of all five ant species studied consist of chambers excavated in the soil, with variation on external appearance from inconspicuous holes in the ground to entrances surrounded by mounds of excavated soil pellets. S. saussurei was mainly nocturnal, M. morschi was active all day, and the other species presented diurnal activity. All species foraged exclusively on the ground and near their nests. All five species collected substrates of animal origin (mainly arthropod feces) and vegetable matter on which to cultivate their fungus gardens. Data on basic biological features of these ants, which represent phylogenetically diverse lineages, contribute to a better understanding of their mutualistic relationships with their fungal symbionts and of the evolutionary processes that produced the derived characteristics in the subtribe Attina. Additionally, this study adds to our knowledge of the natural history of fungus-farming ants in Atlantic rainforest and increases our understanding of their roles in this threatened biome.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Bochynek T, Tanner JL, Meyer B, Burd M (2017) Parallel foraging cycles for different resources in leaf-cutting ants: a clue to the mechanisms of rhythmic activity. Ecol Entomol 42:849–852

    Article  Google Scholar 

  • Bollazzi M, Kronenbitter J, Roces F (2008) Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia 158:165–175

    Article  Google Scholar 

  • Bolton B (2014) An online catalog of the ants of the World. http://antcat.org. Accessed 3 Sept 2018

  • Branstetter MG, Ješovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC, Brady SG, Schultz TR (2017) Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc R Soc B 284:20170095

    Article  Google Scholar 

  • Caldato N, Forti LC, Bouchebti S, Lopes JFS, Fourcassié V (2016) Foraging activity pattern and herbivory rates of the grass-cutting ant Atta capiguara. Insectes Soc 63:421–428

    Article  Google Scholar 

  • Calenge C (2006) The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519

    Article  Google Scholar 

  • Cardoso DC, Cristiano MP, Tavares MG (2011) Methodological remarks on rearing basal Attini ants in the laboratory for biological and evolutionary studies: overview of the genus Mycetophylax. Insectes Soc 58:427–430

    Article  Google Scholar 

  • Cherrett JM (1968) The foraging behavior of Atta cephalotes. J Anim Ecol 37:387–403

    Article  Google Scholar 

  • Christianini AV, Oliveira PS (2009) The relevance of ants as seeds rescuers of a primarily Bird-dispersed tree in the Neotropical cerrado savanna. Oecologia 160:735–745

    Article  Google Scholar 

  • Corrêa MM, Silva PSD, Wirth R, Tabarelli M, Leal IR (2010) How leaf-cutting ants impact forests: drastic nest effects on light environment and plant assemblages. Oecologia 162:103–115

    Article  Google Scholar 

  • De Fine Licht HH, Boomsma JJ (2010) Forage collection, substrate preparation, and diet composition in fungus-farming ants. Ecol Entomol 35:259–269

    Article  Google Scholar 

  • Della Lucia TMC, Gandra LC, Guedes RNC (2013) Managing leaf-cutting ants: peculiarities trends and challenges. Pest Manag Sci 70:14–23

    Article  Google Scholar 

  • Diehl-Fleig E, Diehl E (2007) Nest architecture and colony size of the fungus-farming ant Mycetophylax simplex Emery, 1888 (Formicidae, Attini). Insectes Soc 54:242–247

    Article  Google Scholar 

  • Farji-Brener AG, Illes AE (2000) Do leaf-cutting ant nest make “bottom-up” gaps in Neotropical rain forests? A critical review of the evidence. Ecol Lett 3:219–227

    Article  Google Scholar 

  • Feener DH Jr, Moss KAG (1990) Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment. Behav Ecol Sociobiol 26:17–29

    Article  Google Scholar 

  • Fernández F, Sendoya S (2004) List of Neotropical ants (Hymenoptera: Formicidae). Biota Colomb 5:3–93

    Google Scholar 

  • Fernández-Marín H, Zimmerman JK, Wcislo WT (2004) Ecological traits and evolutionary sequence of nest establishment in fungus-farming ants (Hymenoptera, Formicidae, Attini). Biol J Linn Soc 81:39–48

    Article  Google Scholar 

  • Fernández-Marín H, Zimmerman JK, Wcislo WT, Rehner SA (2005) Colony foundation, nest architecture and demography of a basal fungus-farming ant, Mycocepurus smithii (Hymenoptera, Formicidae). J Nat Hist 39:1735–1743

    Article  Google Scholar 

  • Gotelli NJ, Ellison AM (2011) Princípios de estatística em ecologia. Artmed, Porto Alegre

    Google Scholar 

  • Herz H, Beyschlag W, Hölldobler B (2007) Herbivory rate of leaf-cutting ants in a tropical moist forest in Panama at the population and ecosystem scales. Biotropica 39:482–488

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Hölldobler B, Wilson EO (2011) The leafcutter ants: civilization by instinct. W.W Norton and Company, New York

    Google Scholar 

  • Ješovnik A, Sosa-Calvo J, Lopes CT, Vasconcelos HL, Schultz TR (2013) Nest architecture, fungus gardens, queen, males and larvae of the fungus-growing ant Mycetagroicus inflatus Brandão & Mayhé-Nunes. Insectes Soc 60:531–542

    Article  Google Scholar 

  • Ješovnik A, González VL, Schultz TR (2016) Phylogenomics and divergence dating of fungus-farming ants (Hymenoptera: Formicidae) of the genera Sericomyrmex and Apterostigma. PLoS One 11:e0151059

    Article  Google Scholar 

  • Ješovnik A, Schultz TR (2017) Revision of the fungus-farming ant genus Sericomyrmex Mayr (Hymenoptera, Formicidae, Myrmicinae). ZooKeys 670:1–109

    Article  Google Scholar 

  • Ješovnik A, Chaul J, Schultz T (2018) Natural history and nest architecture of the fungus-farming ant genus Sericomyrmex (Hymenoptera: Formicidae). Myrmecol News 26:65–80

    Google Scholar 

  • Joly CA, Martinelli LA, Alves LF, Vieira SA, Tamashiro JY, Aidar MPM, Camargo PB, Assis MA, Bernacci LC, Durigan G (2008) As parcelas permanentes do projeto temático Biota Gradiente Funcional: composição florística, estrutura e funcionamento da floresta ombrófila densa dos Núcleos Picinguaba e Santa Virgínia do Parque Estadual da Serra do Mar, Estado de São Paulo, Brasil. In: Sanquetta CR (ed) Experiências de monitoramento no Bioma Mata Atlântica com uso de parcelas permanentes. Funpar, Curitiba, pp 109–129

    Google Scholar 

  • Klingenberg C, Brandão CRF, Engels W (2007) Primitive nest architecture and small monogynous colonies in basal Attini inhabiting sandy beaches of southern Brazil. Stud Neotrop Fauna Environ 42:121–126

    Article  Google Scholar 

  • Klingenberg C, Brandão CRF (2009) Revision of the fungus-growing ant genera Mycetophylax Emery and Paramycetophylax Kusnezov rev. stat., and description of Kalathomyrmex n. gen. (Formicidae: Myrmicinae: Attini). Zootaxa 2052:1–31

    Article  Google Scholar 

  • Leal IR (1998) Ecologia e história natural de formigas Attini em vegetação do Cerrado, PhD thesis. Instituto de Biologia, Universidade Estadual de Campinas, Campinas

    Google Scholar 

  • Leal IR, Oliveira PS (1998) Interactions between fungus growing ants (Attini), fruits and seeds in Cerrado vegetation in Southeast Brazil. Biotropica 30:170–178

    Article  Google Scholar 

  • Leal IR, Oliveira PS (2000) Foraging ecology of attine ants in Neotropical savannah: seasonal use of fungal substrate in the Cerrado vegetation of Brazil. Insectes Soc 47:376–382

    Article  Google Scholar 

  • Leal IR, Silva PSD, Oliveira PS (2011) Natural history and ecological correlates of fungus-farming ants (Formicidae: Attini) in the Neotropical Cerrado Savanna. Ann Entomol Soc Am 104:901–908

    Article  Google Scholar 

  • Leal IR, Wirth R, Tabarelli M (2014) The multiple impacts of leaf-cutting ants and their novel ecological role in human-modified neotropical forests. Biotropica 46:516–528

    Article  Google Scholar 

  • Lewis T, Pollard GV, Dibley GC (1974) Micro-environmental factors affecting diel patterns of foraging in the leaf cutting ant Atta cephalotes (L.) (Formicidae: Attini). J Anim Ecol 43:143–153

    Article  Google Scholar 

  • Li H, Sosa-Calvo J, Horn HA, Pupo MT, Clardy J, Rabeling C, Schultz TR, Currie CR (2018) Convergent evolution of complex structures for ant–bacterial defensive symbiosis in fungus-farming ants. Proc Natl Acad Sci 115:10725

    Google Scholar 

  • Mayhé-Nunes AJ, Jaffé K (1998) On the biogeography of Attini (Hymenoptera: Formicidae). Ecotropicus 11:45–54

    Google Scholar 

  • Mayhé-Nunes AJ, Brandão CRF (2006) Revisionary notes on the fungus-farming ant genus Mycetarotes Emery (Hymenoptera, Formicidae). Rev Bras Entomol 50:463–472

    Article  Google Scholar 

  • Mehdiabadi NJ, Schultz TR (2009) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecol News 13:37–55

    Google Scholar 

  • Montoya-Lerma J, Giraldo-Echeverri C, Armbrecht I, Farji-Brener A, Calle Z (2012) Leaf-cutting ants revisited: towards rational management and control. Int J Pest Manag 58:225–247

    Article  Google Scholar 

  • Moreira A, Forti LC, Andrade AP, Boaretto MAC, Lopes JFS (2004) Nest Architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud Neotrop Fauna Environ 39:109–116

    Article  Google Scholar 

  • Mueller UG, Schultz TR, Currie CR, Adams RM, Malloch D (2001) The origin of the Attine ant-fungus mutualism. Q Rev Biol 76:169–197

    Article  CAS  Google Scholar 

  • Mueller UG, Wcislo WT (1998) Nesting biology of the fungus-farming ant Cyphomyrmex longiscapus Weber (Attini, Formicidae). Insectes Soc 45:181–189

    Article  Google Scholar 

  • Nehring V, Boomsma JJ, d’Ettorre P (2012) Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants. Curr Biol 22:R671–R673

    Article  CAS  Google Scholar 

  • Ness J, Mooney K, Lach L (2010) Ants as mutualists. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, Oxford, pp 97–114

    Google Scholar 

  • Oliveira PS, Galetti M, Pedroni F, Morellato LPC (1995) Seed cleaning by Mycocepurus goeldii ants (Attini) facilitates germination in Hymenaea courbaril (Caesalpiniaceae). Biotropica 27:518–522

    Article  Google Scholar 

  • Orr MR (1992) Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant, Atta cephalotes (Hymenoptera. Formicidae). Behav Ecol Sociobiol 30:395–402

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 4 Sept 2018

  • Rabeling C, Verhaagh M, Engels W (2007) Comparative study of the nest architecture and colony structure of the fungus-farming ants, Mycocepurus goeldii and Mycocepurus smithii. J Insect Sci 7:1–13

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Ronque MUV, Migliorini GH, Oliveira PS (2018) Thievery in rainforest fungus-growing ants: interspecific assault on culturing material at nest entrance. Insectes Soc 65:507–510

    Article  Google Scholar 

  • Röschard J, Roces F (2003) Cutters, carriers and transport chains: distance-dependent foraging strategies in the grass-cutting ant Atta vollenweideri. Insectes Soc 50:237–244

    Article  Google Scholar 

  • San Martin-Gajardo I, Morellato LP (2003) Fenologia de Rubiaceae de sub-bosque em floresta Atlântica no sudeste do Brasil. Rev Bras Bot 26:299–309

    Article  Google Scholar 

  • Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440

    Article  CAS  Google Scholar 

  • Silva PD, Leal IR, Wirth R, Tabarelli M (2007) Harvesting of Protium heptaphyllum (Aubl.) March. seeds (Burseraceae) by leaf-cutting ant Atta sexdens L. promotes seed aggregation and seedling mortality. Rev Bras Bot 30:553–560

    Article  Google Scholar 

  • Seal JN, Tschinkel WR (2008) Food limitation in the fungus-gardening ant, Trachymyrmex septentrionalis. Ecol Entomol 33:597–607

    Article  Google Scholar 

  • Solomon SE, Mueller UG, Schultz TR, Currie CR, Price SL, Oliveira da Silva-Pinhati AC, Bacci M Jr, Vasconcelos HL (2004) Nesting biology of the fungus growing ants Mycetarotes Emery (Attini, Formicidae). Insectes Soc 51:333–338

    Article  Google Scholar 

  • Solomon SE, Lopes CT, Mueller UG et al (2011) Nesting biology and fungiculture of the fungus-growing ant, Mycetagroicus cerradensis: new light on the origin of higher attine agriculture. J Insect Sci 11:1–14

    Article  Google Scholar 

  • Sosa-Calvo J, Schultz TR, Brandão CRF et al (2013) Cyatta abscondita: taxonomy, evolution, and natural history of a new fungus-farming ant genus from Brazil. PLoS One 8:e80498

    Article  Google Scholar 

  • Sosa-Calvo J, Ješovnik A, Okonski E, Schultz TR (2015) Locating, collecting, and maintaining colonies of fungus-farming ants (Hymenoptera: Myrmicinae: Attini). Sociobiology 62:300–320

    Article  Google Scholar 

  • Sosa-Calvo J, Ješovnik A, Vasconcelos HL, Bacci M Jr, Schultz TR (2017) Rediscovery of the enigmatic fungus-farming ant “Mycetosoritis” asper Mayr (Hymenoptera: Formicidae): implications for taxonomy, phylogeny, and the evolution of agriculture in ants. PLoS One 12:e0178498

    Article  Google Scholar 

  • Sosa-Calvo J, Schultz TR, Ješovnik A, Dahan RA, Rabeling C (2018) Evolution, systematics, and natural history of a new genus of cryptobiotic fungus-growing ants. Syst Entomol 43:549–567

    Article  Google Scholar 

  • Sternberg LD, Pinzon MC, Moreira MZ, Moutinho P, Rojas EI, Herre EA (2007) Plants use macronutrients accumulated in leaf-cutting ant nests. Proc R Soc B 274:315–321

    Article  CAS  Google Scholar 

  • Verza SS, Forti LC, Lopes JFS, Hughes WOH (2007) Nest architecture of the leaf-cutting ant Acromyrmex rugosus rugosus. Insectes Soc 54:303–309

    Article  Google Scholar 

  • Waller DA (1989) Foraging behaviour of Trachymyrmex turrifex Wheeler (Formicidae: Attini). Southwestern Nat 34:271–275

    Article  Google Scholar 

  • Ward PS, Brady SG, Fisher BL, Schultz TR (2015) The evolution of Myrmicinae ants: phylogeny and biogeography of hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol 40:61–81

    Article  Google Scholar 

  • Weber NA (1937) The biology of the fungus-growing ants Part 1. New forms. Rev Entomol 7:378–409

    Google Scholar 

  • Weber NA (1941) The biology of the fungus-farming ants. Part VII. The Barro Colorado Island, Canal Zone, species. Rev Entomol 12:93–130

    Google Scholar 

  • Weber NA (1966) Fungus-farming ants. Science 153:587–604

    Article  CAS  Google Scholar 

  • Weber NA (1969) A comparative study of the nests, gardens and fungi of the fungus-growing ants, Attini. VI Congress of IUSSI, Bern, pp 299–307

    Google Scholar 

  • Weber NA (1972) Gardening ants, the attines. Memoirs of the American Philosophical Society, Philadelphia, 146 pp

    Google Scholar 

  • Weber NA (1982) Fungus ants. In: Hermann HR (ed) Social insects, vol IV. Academic Press, New York, pp 255–363

    Chapter  Google Scholar 

  • Wetterer JK (1995) Forager size and ecology of Acromyrmex coronatus and other leaf-cutting ants in Costa Rica. Oecologia 104:409–415

    Article  Google Scholar 

  • Wetterer JK, Gruner DS, Lopez JE (1998) Foraging and nesting ecology of Acromyrmex octospinosus (Hymenoptera: Formicidae) in a Costa Rican tropical dry forest. Fla Entomol 81:61–67

    Article  Google Scholar 

  • Wheeler WM (1925) A new guest-ant and other new Formicidae from Barro Colorado Island, Panama. Biol Bull 49:150–184

    Article  Google Scholar 

  • Wilson EO (1980) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Behav Ecol Sociobiol 7:143–156

    Article  Google Scholar 

  • Wirth W, Herz H, Ryel RJ, Beyschlag W, Hölldobler B (2003) Herbivory of leaf-cutting ants: a case study on Atta colombica in the Tropical Rainforest of Panama. Ecol Stud 164:1–230

    Article  Google Scholar 

Download references

Acknowledgements

We thank Ted Schultz for valuable comments on the manuscript. The Parque Estadual Serra do Mar (Núcleo Picinguaba) and the Instituto Florestal do Estado de São Paulo provided logistic support, and Eliane Rodrigues gave permission to work at the Pousada Betânia. We thank G.H. Migliorini and A. Tacioli for helping during fieldwork, A. Ješovnik for identifying the Sericomyrmex species, H. Soares Jr. for helping with the photos; A.V. Christianini, F.B. Noll and M.S.C. Morini for comments at early stages of the study. M.U.V R. was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), R.M.F. was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 302462/2016-3), and P.S.O. was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 306115/2013-1, 302219/2017-0) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2014/23141-1, 2017/16645-1).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to M. U. V. Ronque or P. S. Oliveira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ronque, M.U.V., Feitosa, R.M. & Oliveira, P.S. Natural history and ecology of fungus-farming ants: a field study in Atlantic rainforest. Insect. Soc. 66, 375–387 (2019). https://doi.org/10.1007/s00040-019-00695-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-019-00695-y

Keywords

Navigation