Abstract
How foraging trails are formed and the chemical communication between individual ants is well known. However, communication between partners in mutualistic relationships, such as the leaf-cutting ants (LCA) and their symbiotic fungus, is less studied. There is a feedback mechanism that operates in LCA colonies, with the fungus garden communicating its condition to the ants, most probably using chemicals. We discuss the literature on the chemistry of the LCA–forage–fungus system starting from selection of plants and its effect on the fungus garden. We suggest, using chemical examples, how the fungus might communicate with attendant ants and suggest areas for future research into this fascinating and complex system.
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Introduction
The success of ant societies depends on the foraging workers selecting the most appropriate foods that are nutritive and non-toxic (Hölldobler and Wilson 1990). Many species of ants collect food and feed it directly to conspecifics and brood, with minimal processing, for example, the prey of army ants (Gotwald Jr. 1995), aphid honeydew gathered by mutualist species (Fischer et al. 2001) or detritus collected by omnivorous ants (McGlynn et al. 2009). Some ants collect seeds, which are propagated in nutrient-rich soils in so-called “ant gardens”, with ants feeding on the plant tissue (Davidson 1988; Chomicki and Renner 2016). Other ants, such as fungus farming ants from the sub-tribe Attina (tribe Attini), use fungal symbionts to digest plant material and the ants then feed on the fungal structures, rather than the foraged material: in essence the insects are “farming” the fungus (Mehdiabadi and Schultz 2010; Hölldobler and Wilson 2011).
The most derived form of fungus farming by ants involves the cultivation of Leucoagaricus gongylophorus (Singer 1986) by leaf-cutting ants (LCA) within the genera Atta (Fabricius 1804) (At.) and Acromyrmex (Mayr 1865) (Ac.) (Mehdiabadi and Schultz 2010). There is a great deal of evidence that this system is co-ordinated by chemical signals, but in comparison with other aspects of ant biology there is a lot more to discover. This ant–fungus chemical interaction is likely to involve a range of chemical signals—semiochemicals—including allomones, kairomones and synomones (see Beck et al. 2017). It is known that compounds produced by L. gongylophorus can cause growth of pathogens towards the fungus (Folgarait et al. 2011; Masiulionis et al. 2015; Birnbaum and Gerardo 2016). We focus on the chemical communications between the foraged plant material, the LCAs and the fungus garden highlighting what is known and where there are gaps in knowledge.
Leaf-cutting ant biology and essential conditions for the fungus garden
The LCAs consist of ca. 40 described species and are major defoliating herbivores in the New World impacting upon plant community structure (Hölldobler and Wilson 1990; Costa et al. 2008; Mehdiabadi and Schultz 2010; Leal et al. 2014). Fungus-growing ants evolved approximately 60 MYA, with recent evidence suggesting that extant LCAs evolved around 19 MYA in dry habitats in Central America (Branstetter et al. 2017). The key to the success of LCA is the highly evolved mutualistic association between the ants and their fungal symbiont, L. gongylophorus (Ridley et al. 1996; North et al. 1997; Schultz and Brady 2008). The fungus is cultivated on pulped leaf material supplemented by faeces (Hölldobler and Wilson 1990), to form the so-called “fungus gardens”. Swollen hyphal tips—gongylidia—are a unique fungal adaptation and provide the sole food source for the ants and their developing brood (Hölldobler and Wilson 2011).
Complex assemblages of beneficial microorganisms contribute to the health of the colony with actinomycetous bacteria, e.g. Pseudonocardia, used as a source of antibiotics by LCAs (Poulsen et al. 2007; Sen et al. 2009) while other bacteria fix nitrogen, increasing the productivity of the colony (Pinto-Tomás et al. 2009). Yeasts, while not generally regarded as essential, appear to contribute to degradation of plant materials and detoxification of potentially harmful compounds, such as galacturonic acid (Mendes et al. 2012). The fungal garden is propagated and maintained by hygienic behaviour (Fernandez-Marin et al. 2006; Mangone and Currie 2007; Della Lucia et al. 2014). For example, the metapleural gland secretion from ants contains antimicrobial compounds, such as phenyl acetic acid (Fernández-Marín et al. 2015), which restrict the growth of fungal and bacterial pathogens (Ortius-Lechner et al. 2000), such as the microfungus Escovopsis (Ascomycota: Hypocreales) (Currie et al. 1999; Haeder et al. 2009). The ants’ hygienic behaviour is very effective as the fungal garden does not persist if the ants are removed (Weber 1966; Mueller et al. 2005).
Maintenance of the microbiome is important for the health of the fungal garden but the primary factor affecting the growth of the gongylidia is the collection and preparation of a suitable substrate by foragers. Foraging trails can be highly adaptable to make use of the most nutritious and least toxic plant material within constantly changing environments (Silva et al. 2013). Some LCAs are specialist foragers on either mono- or dicotyledonous plant species (e.g. Pereira et al. 2016), although within this range of acceptability suitable plant material is collected based upon its physical (Cherrett 1972; Nichols-Orians and Schultz 1989; Bollazzi et al. 2011) and chemical properties (Hubbell et al. 1984; Howard 1987, 1988).
Factors governing selection of plants
Nutrients
The acceptance of plant material can be affected by leaf nutrients, and young leaves with higher concentrations of phosphorous, potassium or nitrogen are collected by At. cephalotes (L.) (Linnaeus 1758) (Berish 1986) and At. laevigata (Smith 1858) (Mundim et al. 2009), whereas At. colombica (Guérin-Méneville 1844) selects drought-stressed leaves, that contain a greater concentration of carbohydrates and proline (Meyer et al. 2006). Production of cellulolytic and carbohydrate-active enzymes by the microorganisms associated with fungus gardens varies between Atta and Acromyrmex, and this difference could be an adaptation to decomposition of the plant material foraged (Suen et al. 2010; Kooij et al. 2014, 2015).
Secondary compounds
Within plant tissues, the mixture of either constitutive or induced secondary compounds can be a reliable predictor of plant utilization by LCA (Howard 1987, 1988, 1990; Howard et al. 1989). In general, compounds or mixtures of compounds from plants can attract or repel insects, acting as “push–pull” stimuli (Cook et al. 2007). In relation to the “pull” effect, some volatile compounds can attract LCAs in laboratory studies (Perri et al. 2017) but it is unclear how these compounds act in natural situations. There is more information on repellent and toxic compounds. Some examples, mainly from laboratory bioassays, have shown that LCAs can be repelled by plant chemical defences induced by mechanical damage or by hormones, such as jasmonic acid (Kost et al. 2011). Constitutive plant compounds prevent collection of leaves since At. sexdens rubropilosa (Forel 1908) does not feed on leaves of Ricinis communis L. (Euphorbiaceae) under natural conditions, which is probably due to a mixture of fatty acids and the presence of an ant toxin, ricinine (Bigi et al. 2004) and At. cephalotes will avoid plant leaves containing high levels of toxic saponins (Folgarait et al. 1996).
It has been suggested that At. cephalotes are more common where young or “pioneer” plants predominate, rather than in more mature or established neotropical forest, because young and pioneer plants have lower levels of protective—toxic or repellent—chemicals (Farji-Brener 2001). These findings are supported by laboratory bioassays, where discs cut from young leaves were selected in preference to old leaves both by At. cephalotes and Ac. octospinosus (Reich) (Littledyke and Cherrett 1975, 1978).
Endophytes and plant fungal pathogens
Plants produce their own chemical defences, but this can be modulated by the presence of benign endophytes that do not cause disease but alter plant physiology so that asymptomatic cucumber leaves inoculated with a single species of endophyte emit compounds associated with damage, such as β-ocimene and 4,8-dimethyl-1,3,7-nonatriene which can repel ants (Estrada et al. 2013). It is also possible that LCAs select plant materials based upon the compatibility of the endophyte community with the fungal garden (Van Bael et al. 2011; Estrada et al. 2014, 2015).
Pathogenic fungi also induce chemical changes in plants. As a selected cohort of 42 plants in the dry forest of Costa Rica became more infected with fungal pathogens in the wet season, they produced more phytoalexins which repelled At. cephalotes foragers (Hubbell et al. 1984). Among these compounds, there were sesquiterpenes and triterpenes in the leaves of Cordia alliodora (Ruiz and Pav) Oken (Boraginaceae) and Verbesina gigantea Jacq. (Asteraceae), which were found to be repellent at naturally occurring concentrations (Chen et al. 1983; Hubbell and Wiemer 1983; Hubbell et al. 1984).
Imperfect foraging and the need for feedback
Free-living ants self-select forage in an attempt to optimize its preparation for growth of fungal monocultures (De Fine Licht and Boomsma 2010), but if ants have not encountered and foraged a plant before, collection and transport back to the fungal garden is driven by acceptability of the material to the ants (Rockwood and Hubbell 1987). Foragers are able to detect and rapidly reject plants that contain compounds toxic or repellent to the ants (Seal and Tschinkel 2007). Some plants that repel ants also retard growth of the fungus (Diaz Napal et al. 2015) and individual compounds (e.g. caffeine) inhibit the growth of fungi and can explain why At. sexdens rubropilosa forages low-caffeine varieties of Coffea sp. (Miyashira et al. 2012). Other plants with mycostatic effects in vitro are those that are not foraged upon (Lapointe et al. 1996). For example, Virola sebifera Aubl. (Myristicaceae) is not collected by At. sexdens rubropilosa and this may be due to lignans, which show fungistatic effects in the laboratory (Pagnocca et al. 1996).
Although leaf-cutting ants assess the suitability of plant material, we know that foraging is imperfect as what LCAs select and incorporate into the fungal garden may not always be optimal for the growth of the fungus (Herz et al. 2008). Some extracts of plants, plant compounds and synthetic molecules can be toxic to the fungus, but neither toxic nor repellent to the ants (Ambrozin et al. 2006; Bigi et al. 2004; Bueno et al. 2005; Howard et al. 1988; Pagnocca et al. 1990, 1996, 2006; Victor et al. 2001). So, survival of the colony in circumstances where ants make a wrong decision then depends on effective communication between the fungal garden and the attendant ants.
Delayed responses and learning
Once plant material is taken back to the nest, the response of the ants to mycotoxic compounds in particular can be delayed (Saverschek et al. 2010; Saverschek and Roces 2011) termed “delayed rejection” (Ridley et al. 1996). For example, there are some plants in the habitat of Ac. ambiguus (Emery 1888) that are not collected as they are unsuitable for the fungus garden (Saverschek et al. 2010). However, colonies of Ac. ambiguus that had not previously been exposed to these plants did not reject immediately (Saverschek and Roces 2011). When Ac. ambiguus were provided with plant material treated with undetectable fungicide, they learned to associate plant odours and cues from damaged fungi with the foraged leaves, which caused rejection in behavioural experiments (Arenas and Roces 2016a, b). This rejection is thought to be due to volatile signals, re-enforced by close contact with leaf surfaces (Saverschek et al. 2010; Saverschek and Roces 2011). Under no-choice laboratory conditions At. sexdens (Linnaeus 1758) foragers will collect leaves of Sesamum indicum L. (Pedaliaceae) and although the leaves eventually repel ants the colony cannot recover (Bueno et al. 1995), due at least in part to a mixture of fatty acids which are toxic to the fungus when combined (Ribeiro et al. 1998). This suggests that there is some chemical change in the fungus as it utilizes the resource due to plant toxins and which is perceived by the ants within the fungal garden (Herz et al. 2008; Thiele et al. 2014). Chemicals are transferred between At. sexdens rubropilosa and the fungus colony by direct contact (North et al. 1999), which may take the form of chemically marking acceptable food (Bradshaw et al. 1986) or by antennal contact between workers (Lenoir 1982).
Detection of changes in the fungal garden
We argue that based upon the perception of chemicals emitted by fungal gardens LCAs are able to distinguish between healthy and disturbed or degrading colonies, based upon characteristics of the strain of fungus that they cultivate and the chemical compounds produced by other organisms in the microbiome, and are able to detect perturbations in the chemical profile. Production of primordia by the fungal garden would reduce somatic growth and the nutrients available to the colony and be perceived by ants as a change in the chemistry of the fungus. Reproduction of the fungus is suppressed by the activities of ants (Pagnocca et al. 2001) and the presence of these mushrooms is usually a symptom that the colony is in decline (Fisher et al. 1994a, b). Of more immediate significance for the survival of the colony is fungal distress or death due to toxins or pathogens. North et al. (1999) suggest that as the fungus dies it produces breakdown products and these compounds act as semiochemicals. Ants that self-select and take many different types of forage back to the nest create a patchwork of different plant materials in the fungal garden. In nests of At. sexdens rubropilosa, this is manifested as unequal production of staphylae—clusters of gongylidia—by the fungal garden (Camargo et al. 2008) and may be what the ants detect. In a healthy colony, a first response of LCAs is to secrete antimicrobial molecules to prevent or halt the spread of pathogens (Fernandez-Marin et al. 2006, 2015) and pathogens are excised by At. colombica (Mighell and van Bael 2016). This ability to discriminate pathogens and mutualists presents the possibility that the pathogenic species causes chemical changes in the fungal garden as it produces enzymes or physical structures that disrupt the gongylidia (Marfetán et al. 2015). The fungal garden that is damaged either by toxic forage or by pathogens is disposed of at the waste dump and there is some research to show that the process of transferring damaged fungi, together with toxic forage to the waste dump, is an important step in the associative learning process, especially for naive worker ants (Arenas and Roces 2016a, b, 2017; Scott et al. 2010).
Fungal compounds governing ant behaviour
As saprotrophs, fungi cause chemical changes in substrates, and this activity can be detected as changes in the chemicals surrounding the fungus, especially as volatiles produced by primary or secondary metabolism (Morath et al. 2012). There is significant evidence that fungi produce semiochemicals which affect physiology, survival and behaviour in many insect taxa (e.g. Davis et al. 2013), including ants (Holighaus and Rohlfs 2016). Mueller et al. (2017) have recently highlighted the diversity of fungal genotypes cultivated by the extant Atta and Acromyrmex, and this is likely to have an effect on the metabolism of the fungi and inter alia the compounds involved in communication with LCAs. In turn, the range of acceptable plant materials and, therefore, the diet breadth of individual colonies, could be driven by the different strains of fungus, as Mueller et al. (2017) suggest. We speculate that these differences, over evolutionary time, may result in greater degrees of fidelity between LCAs and their fungal strains. Colony-specific chemical profiles emitted by the different genotypes of fungi—in particular aldehydes, amides and their methyl esters—contribute to nestmate recognition in Ac. octospinosus nests (Hernandez et al. 2006; Sainz-Borgo et al. 2013). Ants that fed on fungi from colonies other than their own are accepted more readily into the foreign colony (Richard et al. 2007).
So, it is probable that different strains of L. gongylophorus each produce a chemical profile, or signature, which helps to perpetuate associations across lineages of ants. A healthy fungus would not have to invest significant metabolic resources for the maintenance of this chemical signature as it is a consequence of primary metabolism. Induction of stress in the fungus, due to sub-optimal forage or pathogens is likely to alter this chemical signature. Since the fungus would incur a metabolic cost by allocating resources to the production of secondary compounds (Böllmann et al. 2010), we believe that the semiochemicals perceived by ants would be existing metabolites that are up-regulated or that undergo minor structural modification. We further suggest that these compounds would be relatively simple metabolites. For example, the eight carbon oxylipins, derived from peroxidation of lipids constitute a structurally diverse group of fungal compounds with a wide range of ecological functions (Brodhun and Feussner 2011), while in fungi they are involved in growth, development (Tsitsigiannis 2005; Tsitsigiannis and Keller 2006, 2007; Brodhun and Feussner 2011) and as signalling molecules between pathogenic fungi and their plant hosts (Tsitsigiannis and Keller 2007). Furthermore, other molecules of C7 and greater, such as alkanes, aliphatic alcohols, acids and ketones initiate the alarm response of leaf-cutting ants, but occur in varying proportions between Atta and Acromyrmex species (Norman et al. 2017). It would be interesting to investigate if there is some similarity between the blends of molecules that govern recognition of nestmates or that signal alarm in LCAs and stress in fungi.
Conclusions
Plant chemistry determines whether plants are collected by LCAs and, in turn, the effects of this material on the fungal garden modify behaviour of LCAs. Within the nest chemical treatment with secreted molecules, removal of damaged areas and disposal on waste dumps are key behaviours; the process of removal and disposal seems to drive colony learning. Exactly how the fungus communicates either distress as it is damaged or a change in reproductive state and which compounds are involved and the genetic basis of their production are not yet known. Collection, extraction, analysis and bioassay of fungal compounds associated with Atta and Acromyrmex would start to piece together their role and how they convey information.
References
Ambrozin ARP, Leite AC, Bueno FC et al (2006) Limonoids from andiroba oil and Cedrela fissilis and their insecticidal activity. J Braz Chem Soc 17:542–547
Arenas A, Roces F (2016a) Learning through the waste: olfactory cues from the colony refuse influence plant preferences in foraging leaf-cutting ants. J Exp Biol 219:2490–2496
Arenas A, Roces F (2016b) Gardeners and midden workers in leaf-cutting ants learn to avoid plants unsuitable for the fungus at their worksites. Anim Behav 115:167–174
Arenas A, Roces F (2017) Avoidance of plants unsuitable for the symbiotic fungus in leaf-cutting ants: learning can take place entirely at the colony dump. PLoS One 12:e0171388
Beck JJ, Torto B, Vannette RL (2017) Eavesdropping on plant–insect–microbe chemical communications in agricultural ecology: a virtual issue on semiochemicals. J Agric Food Chem 65:S101–S103
Berish CW (1986) Leaf-cutting ants (Atta cephalotes) select nitrogen rich forage. Am Midl Nat 115:268–276
Bigi M, Torkomian VL, de Groote ST et al (2004) Activity of Ricinus communis (Euphorbiaceae) and ricinine against the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae) and the symbiotic fungus Leucoagaricus gongylophorus. Pest Manag Sci 60:933–938
Birnbaum SSL, Gerardo NM (2016) Patterns of specificity of the pathogen Escovopsis across the fungus-growing ant symbiosis. Am Nat 188:52–65
Bollazzi M, Roces F, Núñez J et al (2011) Information needs at the beginning of foraging: grass-cutting ants trade off load size for a faster return to the nest. PLoS One 6:e17667
Böllmann J, Elmer M, Wöllecke J et al (2010) Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiologia 53:107–114
Bradshaw JWS, Howse PE, Baker R (1986) A novel autostimulatory pheromone regulating transport of leaves in Atta cephalota. Animal Behav 34:234–240
Branstetter MG, Jesovnik 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 Biol Sci 284:20170095
Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063
Bueno OC, Hebling MJA, da Silva OA, Matenhauer AMC (1995) Effect of sesame (Sesamum indicum) on nest development of Atta sexdens rubropilosa (Hymenoptera: Formicidae). J Appl Entomol 119:341–343
Bueno FC, Godoy MP, Leite AC et al (2005) Toxicity of Cedrela fissilis to Atta sexdens rubropilosa (Hymenoptera: Formicidae) and its symbiotic fungus. Sociobiology 45:389–399
Camargo RS, Forti LC, Lopes JFS, de Matos CAO (2008) Growth of populations and fungus gardens of Atta sexdens rubropilosa (Hymeoptera, Formicidae) response to foraged substrates. Sociobiology 52:1–11
Chen TK, Ales DC, Baenziger NC, Wiemer DF (1983) Ant-repellent triterpenoids from Cordia alliodora. J Org Chem 48:3525–3531
Cherrett JM (1972) Some factors involved in the selection of vegetable substrate by Atta cephalotes (L.) (Hymenoptera: Formicidae) in tropical rain forest. J Anim Ecol 41:647–660
Chomicki G, Renner SS (2016) Obligate plant farming by a specialized ant. Nat Plants 2:16181
Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400
Costa A, Vasconcelos H, Vieira-Neto EHM, Bruna E (2008) Do herbivores exert top-down effects in Neotropical savannas? Estimates of biomass consumption by leaf-cutter ants. J Veget Sci 19:849–854
Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus growing ants use antibiotic producing bacteria to control garden parasites. Nature 398:701–704
Davidson DW (1988) Ecological studies of neotropical ant gardens. Ecology 69:1138–1152
Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39:840–859
De Fine Licht HH, Boomsma JJ (2010) Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecol Entomol 35:259–269
Della Lucia TMC, Gandra LC, Guedes RNC (2014) Managing leaf-cutting ants: peculiarities, trends and challenges. Pest Manag Sci 70:14–23
Diaz Napal GN, Buffa LM, Nolli LC et al (2015) Screening of native plants from central Argentina against the leaf-cutting ant Acromyrmex lundi (Guerin) and its symbiotic fungus. Ind Crops Prod 76:275–280
Estrada C, Wcislo WT, Van Bael SA (2013) Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol 198:241–251
Estrada C, Rojas EI, Wcislo WT, van Bael SA (2014) Fungal endophyte effects on leaf chemistry alter the in vitro growth rates of leaf-cutting ants` fungal mutualist, Leucocoprinus gongylophorus. Fung Ecol 8:37–45
Estrada C, Degner EC, Rojas EI et al (2015) The role of endophyte diversity in protecting plants from defoliation by leaf-cutting ants. Curr Sci 109:55–61
Farji-Brener AG (2001) Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis. Oikos 92:169–177
Fernandez-Marin H, Zimmerman JK, Rehner SA, Wcislo WT (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc B Biol Sci 273:1689–1695
Fernandez-Marin H, Nash DR, Higginbotham S et al (2015) Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants. Proc R Soc B Biol Sci 282:20150212
Fischer MK, Hoffmann KH, Volkl W (2001) Competition for mutualists in an ant-homopteran interaction mediated by hierarchies of ant attendance. Oikos 92:531–541
Fisher PJ, Stradling DJ, Pegler DN (1994a) Leaf cutting ants, their fungus gardens and the formation of basidiomata of Leucoagaricus gongylophorus. Mycologist 8:128–131
Fisher PJ, Stradling DJ, Pegler DN (1994b) Leucoagaricus basidiomata from a live nest of the leaf-cutting ant Atta cephalotes. Mycol Res 98:884–888
Folgarait PJ, Dyer LA, Marquis RJ, Braker HE (1996) Leaf-cutting ant preferences for five native tropical plantation tree species growing under different light conditions. Entomol Exp Appl 80:521–530
Folgarait PJ, Marfetán JA, Cafaro MJ (2011) Growth and conidiation response of Escovopsis weberi (Ascomycota: Hypocreales) against the fungal cultivar of Acromyrmex lundii (Hymenoptera: Formicidae). Environ Entomol 40:342–349
Gotwald WH Jr (1995) Army ants: the biology of social predation. Cornell University Press, Ithaca, New York, USA
Haeder S, Wirth R, Herz H, Spiteller D (2009) Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Natl Acad Sci USA 106:4742–4746
Hernandez JV, Goitia W, Osio A et al (2006) Leaf-cutter ant species (Hymenoptera: Atta) differ in the types of cues used to differentiate between self and others. Anim Behav 71:945–952
Herz H, Hölldobler B, Roces F et al (2008) Delayed rejection in a leaf-cutting ant after foraging on plants unsuitable for the symbiotic fungus. Behav Ecol 19:575–582
Holighaus G, Rohlfs M (2016) Fungal allelochemicals in insect pest management. Appl Microbiol Biotechnol 100:5681–5689
Hölldobler B, Wilson EO (1990) The ants. Balnap/Harvard, Cambridge
Hölldobler B, Wilson EO (2011) The leafcutter ants (civilisation by instinct). W.W. Norton & Company, New York
Howard JJ (1987) Leafcutting ant diet selection—the role of nutrients, water and secondary chemistry. Ecology 68:503–515
Howard JJ (1988) Leafcutting ant diet selection—relative influence of leaf chemistry and physical features. Ecology 69:250–260
Howard JJ (1990) Infidelity of leafcutting ants to host plants—resource heterogeneity or defense induction. Oecologia 82:394–401
Howard JJ, Cazin J, Wiemer DF (1988) Toxicity of terpenoid deterrents to the leafcutting ant Atta cephalotes and its mutualistic fungus. J Chem Ecol 14:59–69
Howard JJ, Green TP, Wiemer DF (1989) Comparative deterrency of 2 terpenoids to 2 genera of Attine ants. J Chem Ecol 15:2279–2288
Hubbell SP, Wiemer DF (1983) Host plant selection by an Attine ant. In: Jaisson P (ed) Social insects in the tropics, vol 2. University of Paris Press, Paris, pp 133–154
Hubbell SP, Howard JJ, Wiemer DF (1984) Chemical leaf repellency to an Attine ant – seasonal distribution among potential host plant species. Ecology 65:1067–1076
Kooij PW, Liberti J, Giampoudakis K et al (2014) Differences in forage-acquisition and fungal enzyme activity contribute to niche segregation in Panamanian leaf-cutting Ants. PLoS One 9(4):e94284
Kooij PW, Poulsen M, Schiøtt M, Boomsma JJ (2015) Somatic incompatability and genetic structure of fungal crops in sympatric Atta colombica and Acromyrmex echinatior leaf-cutting ants. Fungal Ecol 18:10–17
Kost C, Tremmel M, Wirth R (2011) Do leaf cutting ants cut undetected? Testing the effect of ant-induced plant defences on foraging decisions in Atta colombica. PLoS One 6(7):e22340
Lapointe SL, Serrano MS, Corrales II (1996) Resistance to leafcutter ants (Hymenoptera: Formicidae) and inhibition of their fungal symbiont by tropical forage grasses. J Econ Entomol 89:757–765
Leal IR, Wirth R, Tabarelli M (2014) The multiple impacts by leaf-cutting ants and their novel ecological role in human modified neotropical forests. Biotropica 46:516–528
Lenoir A (1982) An informational analysis of antenall communication during trophallaxis in the ant Myrmica rubra L. Behav Process 7:27–35
Littledyke M, Cherrett JM (1975) Variability in selection of substrate by leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich) (Formicidae, Attini). Bull Entomol Res 65:33–47
Littledyke M, Cherrett JM (1978) Defence mechanisms in young and old leaves against cutting by leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich) (Hymenoptera: Formicidae). Bull Entomol Res 68:263–271
Mangone DM, Currie CR (2007) Garden substrate preparation behaviours in fungus-growing ants. Can Entomol 139:841–849
Marfetán JA, Romero AI, Folgarait PJ (2015) Pathogenic interaction between Escovopsis weberi and Leucoagaricus sp.: mechanisms involved in virulence levels. Fungal Ecol 17:52–61
Masiulionis VE, Cabello MN, Seifert KA et al (2015) Escovopsis trichodermoides sp. nov., isolated from a nest of the lower attine ant Mycocepurus goeldii. Antonie Van Leeuwenhoek 107:731–740
McGlynn TP, Fawcett RM, Clark DA (2009) Litter biomass and nutrient determinants of ant density, nest size, and growth in a Costa Rican tropical wet forest. Biotropica 41:234–240
Mehdiabadi NJ, Schultz TR (2010) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecological News 13:37–55
Mendes TD, Rodrigues A, Dayo-Owoyemi I et al (2012) Generation of nutrients and detoxification: possible roles of yeasts in leaf-cutting ant nests. Insects 3:228–245
Meyer ST, Roces F, Wirth R (2006) Selecting the drought stressed: effects of plant stress on intraspecific and within-plant herbivory patterns of the leaf-cutting ant Atta colombica. Funct Ecol 20:973–981
Mighell K, van Bael SA (2016) Selective elimination of microfungi in leaf-cutting ant gardens. Fung Ecol 24:15–20
Miyashira CH, Tanigushi DG, Gugliotta AM, Santos D (2012) Influence of caffeine on the survival of leaf-cutting ants Atta sexdens rubropilosa and in vitro growth of their mutualistic fungus. Pest Manag Sci 68:935–940
Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83
Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36:563–595
Mueller UG, Ishak HD, Bruschi et al (2017) Biogeography of mutualistic fungi cultivated by leafcutter ants. Mol Ecol 00:1–17
Mundim FM, Costa AN, Vasconcelos HL (2009) Leaf nutrient content and host plant selection by leaf-cutter ants, Atta laevigata, in a Neotropical savanna. Entomol Exp Appl 130:47–54
Nichols-Orians CM, Schultz JC (1989) Leaf toughness affects leaf harvesting by the leaf cutter ant, Atta cephalotes (L.) (Hymenoptera, Formicidae). Biotropica 21:80–83
Norman VC, Butterfield T, Drijfhout F et al (2017) Alarm pheromone composition and behavioral activity in fungus-growing ants. J Chem Ecol 43:225–235
North RD, Jackson CW, Howse PE (1997) Evolutionary aspects of ant-fungus interactions in leaf-cutting ants. Trends Ecol Evol 12:386–389
North RD, Jackson CW, Howse PE (1999) Communication between the fungus garden and workers of the leaf-cutting ant, Atta sexdens rubropilosa, regarding choice of substrate for the fungus. Physiol Entomol 24:127–133
Ortius-Lechner D, Maile R, Morgan ED, Boomsma JJ (2000) Metaplural gland secretion of the leaf-cutter ant Acromyrmex octospinosus: new compounds and their functional significance. J Chem Ecol 26:1667–1683
Pagnocca FC, Dasilva OA, Heblingberaldo MJ et al (1990) Toxicity of sesame extracts to the symbiotic fungus of leaf-cutting ants. Bull Entomol Res 80:349–352
Pagnocca FC, Ribeiro SB, Torkomian VLV et al (1996) Toxicity of lignans to symbiotic fungus of leaf-cutting ants. J Chem Ecol 22:1325–1330
Pagnocca FC, Bacci M Jr, Fungaro MH, Bueno OC, Hebling MJA, Sant`Anna A et al (2001) RAPD analysis of the sexual state and sterile mycelium of the fungus cultivated by the leaf0-cutting ant Acromyrmex hispidus fallax. Mycol Res 105:173–176
Pagnocca FC, Victor SR, Bueno FC et al (2006) Synthetic amides toxic to the leaf-cutting ant Atta sexdens rubropilosa L. and its symbiotic fungus. Agric For Entomol 8:17–23
Pereira JS, Costa RR, Nagamoto NS, Forti LC, Pagnocca FC, Rodrigues A (2016) Comparative analysis of fungal communities in colonies of two leaf-cutting ant species with different substratum preferences. Fungal Ecol 21:68–75
Perri D, Gorostino N, Fernandez P, Buteler M (2017) Plant-based compounds with potential as push-pull stimuli to manage behaviour of leaf-cutting ants. Entomol Exp Appl 163:150–159
Pinto-Tomás MA, Suen AG, Stevenson DM, Chu FST, Cleland WW, Weimer PJ, Currie CR (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123
Poulsen M, Erhardt DP, Molinaro DJ, Lin T-L, Currie CR (2007) Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism. PLoS One 2(9):e960
Ribeiro SB, Pagnocca FC, Victor SR, Bueno OC, Hebling MJ, Bacci M Jr, Silva OA, Fernandes JB, Vieira PC, Silva MFGF. (1998) Activity of sesame leaf extracts against the symbiotic fungus of Atta sexdens L. Ann Soc Entomol Brasil 27:421–426
Richard F-J, Poulsen M, Hefetz A et al (2007) The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants. Behav Ecol Sociobiol 61:1637–1649
Ridley P, Howse PE, Jackson CW (1996) Control of the behaviour of leaf-cutting ants by their “symbiotic” fungus. Experientia 52:631–635
Rockwood LL, Hubbell SP (1987) Host-plant selection, diet diversity, and optimal foraging in a tropical leafcutting ant. Oecologia 74:55–61
Sainz-Borgo C, Leal B, Cabrera A, Hernandez JV (2013) Mandibular and postpharyngeal gland secretions of Acromyrmex landolti (Hymenoptera: Formicidae) as chemical cues for nestmate recognition. Rev Biol Trop 61:1261–1273
Saverschek N, Roces F (2011) Foraging leafcutter ants: olfactory memory underlies delayed avoidance of plants unsuitable for the symbiotic fungus. Anim Behav 82:453–458
Saverschek N, Herz H, Wagner M, Roces F (2010) Avoiding plants unsuitable for the symbiotic fungus: learning and long-term memory in leaf-cutting ants. Anim Behav 79:689–698
Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440
Scott JJ, Budsberg KJ, Suen G et al (2010) Microbial community structure of leaf-cutter ant fungus gardens and refuse dumps. PLoS One 5(3):e9922
Seal JN, Tschinkel WR (2007) Complexity in an obligate mutualism: do fungus-gardening ants know what makes their garden grow? Behav Ecol Sociobiol 61:1151–1160
Sen R, Ishak HD, Estrada D, Dowd SD, Hong E, Mueller UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci USA 106:17 805–817
Silva PSD, Bieber AGD, Knoch TA et al (2013) Foraging in highly dynamic environments: leaf-cutting ants adjust foraging trail networks to pioneer plant availability. Ent Exp Appl 147:110–119
Suen G, Scott JJ, Aylward FO et al (2010) An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genet 6(9):e1001129
Thiele T, Kost C, Roces F, Wirth R (2014) Foraging leaf-cutting ants learn to reject Vitis vinifera ssp vinifera plants that emit herbivore-induced volatiles. J Chem Ecol 40:617–620
Tsitsigiannis DI (2005) Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiol 151:1809–1821
Tsitsigiannis DI, Keller NP (2006) Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans. Mol Microbiol 59:882–892
Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host–fungal communication signals. Trends Microbiol 15:109–118
Van Bael SA, Estrada C, Wcislo WT (2011) Fungal-fungal interactions in leaf-cutting agriculture. Psyche (Stuttg) 2011:9
Victor SR, Crisostoma FR, Bueno FC et al (2001) Toxicity of synthetic piperonyl compounds to leaf-cutting ants and their symbiotic fungus. Pest Manag Sci 57:603–608
Weber NA (1966) Fungus growing ants. Science 153:587–604
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Communicated by Marko Rohlfs.
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Green, P.W.C., Kooij, P.W. The role of chemical signalling in maintenance of the fungus garden by leaf-cutting ants. Chemoecology 28, 101–107 (2018). https://doi.org/10.1007/s00049-018-0260-x
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DOI: https://doi.org/10.1007/s00049-018-0260-x