Abstract
Trail pheromones deposited by ants lead nestmates to food sources. Based on previous evidence that the trail pheromone of the carpenter ant Camponotus modoc originates from the hindgut, our objective in this study was to identify the key component(s) of the pheromone. We collected C. modoc colonies from conifer forests and maintained them in an outdoor enclosure near our laboratory for chemical analyses and behavioral experiments. In gas chromatographic-electroantennographic detection and gas chromatography-mass spectrometric analyses of worker ant hindgut extracts, we identified five candidate components: 2,4-dimethylhexanoic acid, 2,4-dimethyl-5-hexanolide, pentadecane, dodecanoic acid and 3,4-dihydro-8-hydroxy-3,5,7-trimethylisocoumarin. In a series of trail-following experiments, ants followed trails of synthetic 2,4-dimethyl-5-hexanolide, a blend of the five compounds, and hindgut extract over similar distances, indicating that the hexanolide accounted for the entire behavioral activity of the hindgut extract. The hexanolide not only mediated orientation of C. modoc foragers on trails, it also attracted them over distance, indicating a dual function. Further analyses and bioassays with racemic and stereoselectively synthesized hexanolides revealed that the ants produce, and respond to, the (2S,4R,5S)-stereoisomer. The same stereoisomer is a trail pheromone component in several Camponotus congeners, indicating significant overlap in their respective trail pheromone communication systems.
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03 March 2020
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References
Adams ES (1990) Interaction between the ants Zacryptocerus maculatus and Azteca trigona: interspecific parasitization of information. Biotropica 22:200–206
Akre RD, Hansen LD, Myhre EA (1994) Colony size and polygyny in carpenter ants (Hymenoptera: Formicidae ). J Kansas Entomol Soc 67:1–9
Arn H, Städler E, Rauscher S (1975) The electroantennographic detector — a selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Z Naturforsch 30:722–725
Attygalle AB, Kern F, Huang Q, Meinwald J (1998) Trail pheromone of the myrmicine ant Aphaenogaster rudis (Hymenoptera: Formicidae). Naturwissenschaften 85:38–41. https://doi.org/10.1007/s001140050450
Attygalle AB, Morgan ED (1983) Trail pheromone of the ant Tetramorium caespitum L. Naturwissenschaften 70:364–365. https://doi.org/10.1007/BF00990315
Beckers SG, Deneubourg JL, Pasteels JM (1989) Colony size, communication and ant foraging strategy. Psyche 96:239–256. https://doi.org/10.1155/1989/94279
Bestmann HJ, Kern F, Schäfer D, Witschel MC (1992) 3,4-Dihydroisocoumarins, a new class of ant trail pheromones. Angew Chemie Int Ed English 31:795–796. https://doi.org/10.1002/anie.199207951
Bestmann HJ, Haak U, Kern F, Hölldobler B (1995) 2,4-Dimethyl-5-hexanolide, a trail pheromone component of the carpenter ant Camponotus herculeanus. Naturwissenschaften 82:142–144. https://doi.org/10.1007/BF01177276
Bestmann HJ, Liepold B, Kress A, Hofmann A (1999) (2S,4R,5S)-2,4-Dimethyl-5-hexanolide: ants of different species Camponotus can distinguish the absolute configuration of their trail pheromone. Chem Eur J 5:2984–2989
Billen J, Beeckman W, Morgan ED (1992) Active trail pheromone compounds and trail following in the ant Atta sexdens sexdens (Hymenoptera Formicidae). Ethol Ecol Evol 4:197–202. https://doi.org/10.1080/08927014.1992.9525342
Blum MS, Wilson EO (1964) The anatomical source of trail substances in formicine ants. Psyche 71:28–31. https://doi.org/10.1155/1964/43846
Bolton B (1995) A new general catalogue of the ants of the world. Harvard University Press, Cambridge, MA
Cerdá X, van Oudenhove L, Bernstein C, Boulay R (2014) A list of and some comments about the trail pheromones of ants. Nat Prod Commun 9:1115–1122. https://doi.org/10.1177/1934578X1400900813
Chalissery JM, Renyard A, Gries R, Hoefele D, Alamsetti SK, Gries G (2019) Ants sense, and follow, trail pheromones of ant community members. Insects 10:383. https://doi.org/10.3390/insects10110383
Choe DH, Villafuerte DB, Tsutsui ND (2012) Trail pheromone of the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae). PLoS One 7:e45016. https://doi.org/10.1371/journal.pone.0045016
Czaczkes TJ, Castorena M, Schürch R, Heinze J (2017) Pheromone trail following in the ant Lasius niger: high accuracy and variability but no effect of task state. Physiol Entomol 42:91–97. https://doi.org/10.1111/phen.12174
Czaczkes TJ, Grüter C, Ellis L, Wood E, Ratnieks FLW (2013a) Ant foraging on complex trails: route learning and the role of trail pheromones in Lasius niger. J Exp Biol 216:188–197. https://doi.org/10.1242/jeb.076570
Czaczkes TJ, Grüter C, Ratnieks FLW (2015) Trail pheromones: an integrative view of their role in social insect colony organization. Annu Rev Entomol 60:581–599. https://doi.org/10.1146/annurev-ento-010814-020627
Czaczkes TJ, Grüter C, Ratnieks FLW (2013b) Negative feedback in ants: crowding results in less trail pheromone deposition. J R Soc Interface 10:20121009. https://doi.org/10.1098/rsif.2012.1009
Czaczkes TJ, Nouvellet P, Ratnieks FLW (2011) Cooperative food transport in the Neotropical ant, Pheidole oxyops. Insect Soc 58:153–161. https://doi.org/10.1007/s00040-010-0130-1
Czaczkes TJ, Ratnieks FLW (2012) Pheromone trails in the Brazilian ant Pheidole oxyops: extreme properties and dual recruitment action. Behav Ecol Sociobiol 66:1149–1156. https://doi.org/10.1007/s00265-012-1367-7
David CT, Wood DL (1980) Orientation to trails by a carpenter ant, Camponotus modoc (Hymenoptera: Formicidae), in a giant sequoia forest. Can Entomol 112:993–1000. https://doi.org/10.4039/Ent112993-10
Derstine NT, Ohler B, Jimenez SI, Landolt P, Gries G (2017) Evidence for sex pheromones and inbreeding avoidance in select north American yellowjacket species. Entomol Exp Appl 164:35–44
El-Ziady S, Kennedy JS (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli. Proc R Entomol Soc London (A) 31:61–65. https://doi.org/10.1111/j.1365-3032.1956.tb00208.x
Evershed RP, Morgan ED, Cammaerts 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
Evison SEF, Petchey OL, Beckerman AP, Ratnieks FLW (2008) Combined use of pheromone trails and visual landmarks by the common garden ant Lasius niger. Behav Ecol Sociobiol 63:261–267. https://doi.org/10.1007/s00265-008-0657-6
Fourcassié V, Dussutour A, Deneubourg J (2010) Ant traffic rules. J Exp Biol 213:2357–2363. https://doi.org/10.1242/jeb.031237
Gobin B, Peeters C, Billen J, Morgan ED (1998) Interspecific trail following and commensalism between the ponerine ant Gnamptogenys menadensis and the formicine ant Polyrhachis rufipes. J Insect Behav 11:361–369
Greenberg L, Klotz JH (2000) Argentine ant (Hymenoptera: Formicidae) trail pheromone enhances consumption of liquid sucrose solution. J Econ Entomol 93:119–122
Gries R, Khaskin G, Gries G, Bennett RG, King SGG, Morewood P, Slessor KN, Morewood DW (2002) (Z,Z)-4,7-Tridecadien-(S)-2-yl acetate: Sex pheromone of Douglas-fir cone gall midge, Contarinia oregonensis. J Chem Ecol 28:2283–2297. https://doi.org/10.1023/A:1021005517389
Grüter C, Czaczkes TJ, Ratnieks FLW (2011) Decision making in ant foragers (Lasius niger) facing conflicting private and social information. Behav Ecol Sociobiol 65:141–148. https://doi.org/10.1007/s00265-010-1020-2
Guénard B, Weiser MD, Gómez K, Narula N, Economo EP (2017) The global ant biodiversity informatics (GABI) database: synthesizing data on the geographic distribution of ant species (Hymenoptera: Formicidae). Myrmecol News 24:83–89. https://doi.org/10.25849/myrmecol.news_024:083
Hansen LD, Akre RD (1985) Biology of carpenter ants in Washington state. Melanderia 43:i–v 1-61
Hölldobler B (1971) Recruitment behavior in Camponotus socius (Hym. Formicidae). Z Vgl Physiol 75:123–142
Hölldobler B (1999) Multimodal signals in ant communication. J Comp Physiol A 184:129–141
Hölldobler B, Braun U, Gronenberg W, Kirchner WH, Peeters C (1994) Trail communication in the ant Megaponera foetens (Fabr.) (Formicidae, Ponerinae). J Insect Physiol 40:585–593
Hölldobler B, Möglich M, Maschwitz U (1974) Communication by tandem running in the ant Camponotus sericeus. J Comp Physiol 90:105–127
Hölldobler B, Wilson EO (1978) Multiple recruitment systems of African weaver ant Oecophylla longinoda (Latrielle) (Hymenoptera: Formicidae). Behav Ecol Sociobiol 3:19–60
Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, Cambridge, MA
Jackson BD, Wright PJ, Morgan ED (1989) 3-Ethyl-2,5-dimethylpyrazine, a component of the trail pheromone of the ant Messor bouvieri. Experientia 45:487–489. https://doi.org/10.1007/BF01952041
Janicki J, Narula N, Ziegler M, Guénard B, Economo EP (2016) Visualizing and interacting with large-volume biodiversity data using client-server web-mapping applications: the design and implementation of antmaps.org. Ecol Inform 32:185–193. https://doi.org/10.1016/j.ecoinf.2016.02.006
Janssen E, Bestmann HJ, Hölldobler B, Kern F (1995) N,N-Dimethyluracil and actinidine, two pheromones of the ponerine ant Megaponera foetens (Fab.) (Hymenoptera: Formicidae). J Chem Ecol 21:1947–1955. https://doi.org/10.1007/BF02033854
Janssen E, Übler E, Bauriegel L, Kern F, Bestmann HJ, Attygalle AB, Steghaus-Kovac S, Maschwitz U (1997) Trail pheromone of the ponerine ant Leptogenys peuqueti (Hymenoptera: Formicidae): a multicomponent mixture of related compounds. Naturwissenschaften 84:122–125. https://doi.org/10.1007/s001140050360
Kleineidam CJ, Rössler W, Hölldobler B, Roces F (2007) Perceptual differences in trail-following leaf-cutting ants relate to body size. J Insect Physiol 53:1233–1241. https://doi.org/10.1016/j.jinsphys.2007.06.015
Klotz JH (1984) Diel differences in foraging in two ant species. J Kansas Entomol Soc 57:111–118
Klotz JH, Reid BL (1992) The use of spatial cues for structural guideline orientation in Tapinoma sessile and Camponotus pennsylvanicus (Hymenoptera: Formicidae). J Insect Behav 5:71–82
Klotz J, Reid BL, Hamilton J (2000) Locomotory efficiency in ants using structural guidelines (Hymenoptera: Formicidae). Sociobiology 35:79–88
Kohl E, Hölldobler B, Bestmann HJ (2001) Trail and recruitment pheromones in Camponotus socius (Hymenoptera: Formicidae). Chemoecology 11:67–73. https://doi.org/10.1007/PL00001834
Kohl E, Hölldobler B, Bestmann HJ (2003) Trail pheromones and Dufour gland contents in three Camponotus species (C. castaneus, C. balzani, C. sericeiventris: Formicidae, Hymenoptera). Chemoecology 13:113–122. https://doi.org/10.1007/s00049-003-0237-1
Liefke C, Hölldobler B, Maschwitz U (2001) Recruitment behavior in the ant genus Polyrhachis (Hymenoptera, Formicidae). J Insect Behav 14:637–657
Lizon à l’Allemand S, Witte V (2010) A sophisticated, modular communication contributes to ecological dominance in the invasive ant Anoplolepis gracilipes. Biol Invasions 12:3551–3561. https://doi.org/10.1007/s10530-010-9750-7
Menzel F, Blüthgen N (2010) Parabiotic associations between tropical ants: equal partnership or parasitic exploitation? J Anim Ecol 79:71–81. https://doi.org/10.1111/j.1365-2656.2009.01628.x
Menzel F, Pokorny T, Blüthgen N, Schmitt T (2010) Trail-sharing among tropical ants: interspecific use of trail pheromones? Ecol Entomol 35:495–503. https://doi.org/10.1111/j.1365-2311.2010.01206.x
Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–1093. https://doi.org/10.1126/science.1234316
Morgan ED (2008) Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecol News 11:79–90
Morgan ED (2009) Trail pheromones of ants. Physiol Entomol 34:1–17. https://doi.org/10.1111/j.1365-3032.2008.00658.x
Morgan ED, Keegans SJ, Tits J, Wenseleers T, Billen J (2006) Preferences and differences in the trail pheromone of the leaf-cutting ant Atta sexdens sexdens (Hymenoptera: Formicidae). Eur J Entomol 103:553–558. https://doi.org/10.14411/eje.2006.075
Muscedere ML, Johnson N, Gillis BC, Kamhi JF, Traniello JFA (2012) Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata. J Comp Physiol A 198:219–227. https://doi.org/10.1007/s00359-011-0701-2
Peeters C, Ito F (2015) Wingless and dwarf workers underlie the ecological success of ants (Hymenoptera: Formicidae). Myrmecol News 21:117–130
Planqué R, van den Berg JB, Franks NR (2010) Recruitment strategies and colony size in ants. PLoS One 5:1–8. https://doi.org/10.1371/journal.pone.0011664
R Core Team (2018) R: a language and environment for statistical computing. https://www.R-project.org/
Raley CM, Aubry KB (2006) Foraging ecology of pileated woodpeckers in coastal forests of Washington. J Wildl Manag 70:1266–1275
Roces F (1993) Both evaluation of resource quality and speed of recruited leaf-cutting ants (Acromyrmex lundi) depend on their motivational state. Behav Ecol Sociobiol 33:183–189. https://doi.org/10.1007/BF00216599
Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644. https://doi.org/10.1007/s00265-006-0207-z
Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, Ray A, Zwiebel LJ, Bonasio R, Reinberg D, Liebig J, Berger SL (2016) Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351:aac6633. https://doi.org/10.1126/science.aac6633
Staddon B, Everton I (1980) Haemolymph of milkweed bug Oncopeltus fasciatus (Heteroptera: Lygaeidae): inorganic constituents and amino acids. Comp Biochem Physiol 65:371–374
Tilles DA, Wood DL (1982) The influence of carpenter ant (Camponotus modoc) (Hymentoptera: Formicidae) attendance on the development and survival of aphids (Cinara spp.) (Homoptera: Aphididae) in a giant Sequoia forest. Can Entomol 114:1133–1142. https://doi.org/10.4039/Ent1141133-12
Tilles DA, Wood DL (1986) Foraging behaviour of the carpenter ant, Camponotus modoc (Hymenoptera: Formicidae), in a giant sequoia forest. Can Entomol 118:861–867
Traniello JFA (1977) Recruitment behavior, orientation, and the organization of foraging in the carpenter ant Camponotus pennsylvanicus Degeer (Hymenoptera: Formicidae). Behav Ecol Sociobiol 2:61–79
Übler E, Kern F, Bestmann HJ, Hölldobler B, Attygalle AB (1995) Trail pheromone of two formicine ants, Camponotus silvicola and C. rufipes (Hymenoptera: Formicidae). Naturwissenschaften 82:523–525. https://doi.org/10.1007/BF01134489
Van den Dool H, Kratz P (1963) A generalization of retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr A 11:463–471
Vander Meer RK, Alonso LE (1998) Pheromone directed behaviour in ants. In: Vander Meer RK, Breed M, Winston M (eds) Pheromone communication in social insects. Westview press, Boulder, pp 159–192
Visicchio R, Mori A, Grasso DA, Castracani C, Le Moli F (2001) Glandular sources of recruitment, trail, and propaganda semiochemicals in the slave-making ant Polyergus rufescens. Ethol Ecol Evol 13:361–372. https://doi.org/10.1080/08927014.2001.9522767
Welzel KF, Choe DH (2016) Development of a pheromone-assisted baiting technique for argentine ants (Hymenoptera: Formicidae). J Econ Entomol 109:1303–1309. https://doi.org/10.1093/jee/tow015
Wilson EO (1987) Causes of ecological success: the case of the ants. J Anim Ecol 56:1–9
Wilson EO (1965) Trail sharing in ants. Psyche 72:2–7
Wilson EO, Hölldobler B (2005) The rise of the ants: a phylogenetic and ecological explanation. Proc Natl Acad Sci 102:7411–7414. https://doi.org/10.1073/pnas.0502264102
Witte V, Attygalle AB, Meinwald J (2007) Complex chemical communication in the crazy ant Paratrechina longicornis Latreille (Hymenoptera: Formicidae). Chemoecology 17:57–62. https://doi.org/10.1007/s00049-006-0364-6
Acknowledgments
We thank three anonymous reviewers for constructive comments; Michael Gudmundson for field assistance in locating and collecting ant nests; Grady Ott for generously donating plastic bins for housing ants; Adam Blake and Leithen M’Gonigle for statistical and graphics advice; Laurel Hansen and Robert Higgins for assistance in ant identification; and Adriana Ibtisam, Jasper Li, April Lin, Nicholas Low and Zhanata Almazbekova for help with ant care. This research was supported by a MPM graduate entrance scholarship, a Thelma Finlayson graduate entrance scholarship, a Graduate Fellowship from Simon Fraser University and by an Alexander Graham Bell CGSM from the Natural Sciences and Engineering Research Council of Canada (NSERC) to AR. The research was further supported by an NSERC–Industrial Research Chair to GG with Scotts Canada Ltd. as the industrial sponsor.
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Renyard, A., Alamsetti, S.K., Gries, R. et al. Identification of the Trail Pheromone of the Carpenter Ant Camponotus modoc. J Chem Ecol 45, 901–913 (2019). https://doi.org/10.1007/s10886-019-01114-z
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DOI: https://doi.org/10.1007/s10886-019-01114-z