Abstract
Ants communicate using a suite of chemicals with a level of sophistication that is inextricably linked to their ecological dominance. The fungus-growing ants have been the focus of chemical ecology studies for decades, especially the leaf-cutting ants. Some create long, conspicuous foraging trails to harvest fresh vegetation used to sustain large farming systems that feed millions of workers. However, of the ca. 250 fungus-growing ant species, most feed detritus rather than fresh material to their gardens, and colony sizes are tens to hundreds of workers. Colonies within the attine genus Cyphomyrmex use distinct methods of agriculture (i.e., yeast and lower fungus agriculture). We compared compounds found in five species from the yeast-growing Cyphomyrmex rimosus group (C. rimosus and C. salvini) and the lower agriculture Cyphomyrmex wheeleri group (C. costatus, C. longiscapus, C. muelleri). Compounds identified were compared with those reported in the literature and mapped onto the attine-ant phylogeny, and glands of origin suggested. There were 10 compounds across five species and two are known alarm compounds, 1-octen-3-o1 and 3-octanol. Of the six farnesenes detected, the most notable was the diversity of gaster-derived compounds in C. salvini and the high abundance of (3Z, 6E)-α-7-ethylhomofarnesene and α-6-bishomofarnesene in the three C. wheeleri group species. We also found 2,5-dimethyl-3-isoamylpyrazine in the heads of yeast-growing species, an unexpected result because pyrazines are known trail substances in other attines. Our results expand our understanding of semiochemicals found in fungus-growing ants and provides a starting point to generate hypotheses for more extensive comparative studies.
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References
Adams RMM, Longino JT (2007) Nesting biology of the arboreal fungus-growing ant Cyphomyrmex cornutus and behavioral interactions with the social-parasitic ant Megalomyrmex mondabora. Insectes Soc 54:136–143. https://doi.org/10.1007/s00040-007-0922-0
Adams RMM, Jones TH, Jeter AW et al (2012) A comparative study of exocrine gland chemistry in Trachymyrmex and Sericomyrmex fungus-growing ants. Biochem Syst Ecol 40:91–97. https://doi.org/10.1016/j.bse.2011.10.011
Adams RMM, Jones TH, Longino JT et al (2015) Alkaloid venom weaponry of three Megalomyrmex thief ants and the behavioral response of Cyphomyrmex costatus host ants. J Chem Ecol 41:373–385. https://doi.org/10.1007/s10886-015-0565-y
Albuquerque EZ de (2014) Revisao taxonomica e analise filogenetica do grupo Rimosus de Cyphomyrmex (Hymenoptera, Formicidae, Attini). Thesis, Universidade de Sao Paulo
Ali MF, Jackson BD, Morgan ED (2007) Contents of the poison apparatus of some species of Pheidole ants. Biochem Syst Ecol 35:641–651. https://doi.org/10.1016/j.bse.2007.03.025
AntWeb. 2018. Available from http://www.antweb.org. Accessed 3 October 2018
Attygalle AB, Morgan ED (1982) Structures of homofarnesene and bishomofarnesene isomers from Myrmica ants. J Chem Soc Perkin Trans 1:949–951. https://doi.org/10.1039/P19820000949
Attygalle AB, Morgan ED (1984) Chemicals from the glands of ants. Chem Soc Rev 13:245. https://doi.org/10.1039/cs9841300245
Beckers R, Goss S, Deneubourg JL, Pasteels JM (1989) Colony size, communication and ant foraging strategy. Psyche (New York) 96:239–256. https://doi.org/10.1155/1989/94279
Billen J (2006) Signal variety and communication in social insects. Proc Neth Entomol Soc Meet 17:9–25
Billen J (2009) Diversity and morphology of exocrine glands in ants. In: Proceedings of the 19th symposium of the brazilian myrmecological society, Ouro Preto (Brasil), Nov 17–21, 2009, pp 1–6
Billen J (2011) Exocrine glands and their key function in the communication system of social insects. Formos Entomol 31:75–84. https://doi.org/10.6661/TESFE.2011007
Blum MS, Moser JC, Cordero AD (1964) Chemical releasers of social behavior. II. Source and specificity of the odor trail substances in four attine genera. (Hymenoptera: Formicidae). Psyche (New York) 71:1–7. https://doi.org/10.1155/1964/82896
Branstetter MG, Ješovnik A, Sosa-Calvo J et al (2017) Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc R Soc B Biol Sci 284:20170095. https://doi.org/10.1098/rspb.2017.0095
Cammaerts MC, Cammaerts R (1998) Marking of nest entrance vicinity in the ant Pheidole pallidula (Formicidae, Myrmicinae). Behav Process 42:19–31. https://doi.org/10.1016/S0376-6357(97)00058-2
Cammaerts MC, Evershed RP, Morgan ED (1981) Comparative study of the mandibular gland secretion of four species of Myrmica ants. J Insect Physiol 27:225–231. https://doi.org/10.1016/0022-1910(81)90055-X
Cavill GWK, Robertson PL, Brophy JJ et al (1984) Chemical ecology of the meat ant, Iridomyrmex purpureus sens. strict. Insect Biochem 14:505–513. https://doi.org/10.1016/0020-1790(84)90004-0
Crewe RM, Blum MS (1972) Alarm pheromones of the Attini: their phylogenetic significance. J Insect Physiol 18:31–42. https://doi.org/10.1016/0022-1910(72)90062-5
Cross JH, Byler RC, Ravid U et al (1979) The major component of the trail pheromone of the leaf-cutting ant, Atta sexdens rubropilosa Forel. J Chem Ecol 5:187–203. https://doi.org/10.1007/BF00988234
David Morgan E (2009) Trail pheromones of ants. Physiol Entomol 34:1–17. https://doi.org/10.1111/j.1365-3032.2008.00658.x
Evershed RP, Morgan ED, Cammaertst M (1982) 3-Ethyl-2,5-dimethylpyrazine, the trail pheromone from the venom gland of eight species of Myrmica ants. Insect Biochem 12:383–391. https://doi.org/10.1016/j.jksus.2009.12.009
Ferguson-Gow H, Sumner S, Bourke AFG, Jones KE (2014) Colony size predicts division of labour in attine ants. Proc R Soc B Biol Sci 281:20141411. https://doi.org/10.1098/rspb.2014.1411
Francelino MR, Mendonça AL, Do Nascimento RR, Sant’Ana AEG (2006) The mandibular gland secretions of the leaf-cutting ants Atta sexdens sexdens and Atta opaciceps exhibit intercaste and intercolony variations. J Chem Ecol 32:643–656. https://doi.org/10.1007/s10886-005-9020-9
Hogan CT, Jones TH, Zhukova M et al (2017) Novel mandibular gland volatiles from Apterostigma ants. Biochem Syst Ecol 72:56–62. https://doi.org/10.1016/j.bse.2017.04.005
Hughes WO, Howse PE, Goulson D (2001) Mandibular gland chemistry of grass-cutting ants: species, caste, and colony variation. J Chem Ecol 27:109–124. https://doi.org/10.1023/A:1005624101743
Jackson BD, Morgan ED (1993) Insect chemical communication: pheromones and exocrine glands of ants. Chemoecology 4:125–144. https://doi.org/10.1007/BF01256548
Jackson BD, Cammaerts MC, Morgan ED, Attygalle AB (1990) Chemical and behavioral studies on dufour gland contents of Manica rubida (Hymenoptera, Formicidae). J Chem Ecol 16:827–840. https://doi.org/10.1007/BF01016493
Jaffe K, Marcuse M (1983) Nestmate recognition and territorial behaviour in the ant Odontomachus bauri Emery (Formicidae: Ponerinae). Insectes Soc 30:466–481. https://doi.org/10.1007/BF02223978
Jaffe K, Issa S, Sainz-Borgo C (2012) Chemical recruitment for foraging in ants (Formicidae) and termites (Isoptera): a revealing comparison. Psyche (Stuttg). https://doi.org/10.1155/2012/694910
Jones TH, Flournoy RC, Torres JA et al (1999) 3-Methyl-4-phenylpyrrole from the Ants Anochetus kempfi and Anochetus mayri. 2:1343–1345. https://doi.org/10.1021/np990245t
Kempf WW (1965) A revision of the neotropical fungus-growing ants of the genus Cyphomyrmex Mayr. Part II: group of rimosus (Spinola) (Hym. Formicidae). Stud Entomol 8:161–200
Kweskin MP (2004) Jigging in the fungus-growing ant Cyphomyrmex costatus: a response to collembolan garden invaders? Insectes Soc 51:158–162. https://doi.org/10.1007/s00040-003-0712-2
Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161. https://doi.org/10.1007/s10886-009-9695-4
Mehdiabadi NJM, Schultz TR (2009) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae : Myrmicinae: Attini). Myrmecological News 13:37–55
Mehdiabadi NJ, Mueller UG, Brady SG et al (2012) Symbiont fidelity and the origin of species in fungus-growing ants. Nat Commun 3:840. https://doi.org/10.1038/ncomms1844
Morgan ED (2008) Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecological News 11:79–90
Morgan ED, Do Nascimento RR, Keegans SJ, Billen J (1999) Comparative study of mandibular gland secretions of workers of ponerine ants. J Chem Ecol 25:1395–1409. https://doi.org/10.1023/A:1020987028163 doi
Neupert S, DeMilto A, Drijfhout F et al (2018) Host colony integration: Megalomyrmex guest ant parasites maintain peace with their host using weaponry. Anim Behav 139:71–79. https://doi.org/10.1016/j.anbehav.2018.02.021
Norman VC, Hoppe M, Hughes WOH (2014) Old and wise but not size: Factors affecting threat response behaviour and nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Insectes Soc 61:289–296. https://doi.org/10.1007/s00040-014-0355-5
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. https://doi.org/10.1007/s10886-017-0821-4
Ômura H, Kuwahara Y, Tanabe T (2002) 1-Octen-3-ol together with geosmin: New secretion compounds from a polydesmid millipede, Niponia nodulosa. J Chem Ecol 28:2601–2612. https://doi.org/10.1023/A:1021400606217
Richard FJ, Poulsen M, Drijfhout F et al (2007) Specificity in chemical profiles of workers, brood and mutualistic fungi in Atta, Acromyrmex, and Sericomyrmex fungus-growing ants. J Chem Ecol 33:2281–2292. https://doi.org/10.1007/s10886-007-9385-z
Sainz-Borgo C, Leal B, Cabrera A, Hernández JV (2013) Mandibular and postpharyngeal gland secretions of Acromyrmex landolti (Hymenoptera: Formicidae) as chemical cues for nestmate recognition. Rev Biol Trop 61:1261–1273
Salzemann A, Nagnan P, Tellier F, Jaffe K (1992) Leaf-cutting ant Atta laevigata (Formicidae: Attini) marks its territory with colony-specific dufour gland secretion. J Chem Ecol 18:183–196. https://doi.org/10.1007/BF00993752
Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci 105:5435–5440. https://doi.org/10.1073/pnas.0711024105
Silva-Junior EA, Ruzzini AC, Paludo CR et al (2018) Pyrazines from bacteria and ants: Convergent chemistry within an ecological niche. Sci Rep 8:4–10. https://doi.org/10.1038/s41598-018-20953-6
Snelling RR, Longino JT (1992) Revisionary notes on the fungus-growing ants of the genus Cyphomyrmex rimosus group (Hymenoptera: Formicidae: Attini). In: Quintero D, Aiello A (eds) Insects of Panama and Mesoamerica: selected studies. Oxford University Press, Oxford., pp 479–494
Vander Meer RK, Alvarez FM, Lofgren CS (1988) Isolation of the trail recruitment pheromone of Solenopsis invicta. J Chem Ecol 14:825–838. https://doi.org/10.1007/BF01018776
Vieira AS, Morgan ED, Drijfhout FP, Camargo-Mathias MI (2012) Chemical composition of metalpeural gland secretions of fungus-growing and non-fungus-growing ants. J Chem Ecol 38:1289–1297. https://doi.org/10.1007/s10886-012-0185-8
Ward PS, Brady SG, Fisher BL, Schultz TR (2015) The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol 40:61–81. https://doi.org/10.1111/syen.12090
Xu S, Errabeli R, Feener DH et al (2018) Alkyl-dimethylpyrazines in mandibular gland secretions of four Odontomachus ant species (Formicidae: Ponerinae). J Chem Ecol 44:444–451. https://doi.org/10.1007/s10886-018-0948-y
Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev Camb Philos Soc 86:774–791. https://doi.org/10.1111/j.1469-185X.2010.00170.x
Acknowledgements
We thank the staff and researchers at the Smithsonian Tropical Research Institute (STRI) for logistical support, and the Autoridad Nacional del Ambiente y el Mar for permission to sample and export ants. For assistance in the field, we thank participants of the 2015 and 2017 Tropical Behavioral Ecology and Evolution course, organized and financially supported by the University of Copenhagen (2015) and The Ohio State University (2017) in coordination with STRI. Funding for JZS was provided by a Postdoctoral Fellowship from the Smithsonian Institution Competitive Grants Program, and by a Marie Curie International Incoming Fellowship (327940 INSEAME). RMMA was supported by the University of Copenhagen (2015) and The Ohio State University (2017).
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Communicated by Marko Rohlfs.
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Hamilton, N., Jones, T.H., Shik, J.Z. et al. Context is everything: mapping Cyphomyrmex-derived compounds to the fungus-growing ant phylogeny. Chemoecology 28, 137–144 (2018). https://doi.org/10.1007/s00049-018-0265-5
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DOI: https://doi.org/10.1007/s00049-018-0265-5
Keywords
- Cyphomyrmex
- Fungus-farming ants
- Alarm pheromone
- Trail pheromone
- Chemical communication
- Formicidae