Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T06:35:19.810Z Has data issue: false hasContentIssue false
  • English
  • Français

Intra- and inter-specific variation in alarm pheromone produced by Solenopsis fire ants

Published online by Cambridge University Press:  10 December 2017

L. Hu ,
R.R. Balusu ,
W.-Q. Zhang ,
O.S. Ajayi ,
Y.-Y. Lu ,
R.-S. Zeng ,
H.Y. Fadamiro  and
L. Chen
L. Hu
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, PR China
R.R. Balusu
Affiliation:
Department of Entomology & Plant Pathology, Auburn University, Auburn, Alabama 36849, USA
W.-Q. Zhang
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, PR China College of Agriculture, South China Agricultural University, Guangzhou 510642, PR China
O.S. Ajayi
Affiliation:
Department of Entomology & Plant Pathology, Auburn University, Auburn, Alabama 36849, USA
Y.-Y. Lu
Affiliation:
College of Agriculture, South China Agricultural University, Guangzhou 510642, PR China
R.-S. Zeng
Affiliation:
College of Agriculture, South China Agricultural University, Guangzhou 510642, PR China College of Crop Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, PR China
H.Y. Fadamiro
Affiliation:
Department of Entomology & Plant Pathology, Auburn University, Auburn, Alabama 36849, USA
L. Chen*
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, PR China
*
*Author for correspondence Phone/Fax: +86-10-64807780 E-mail: chenli@ioz.ac.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Some fire ants of the genus Solenopsis have become invasive species in the southern United States displacing native species by competition. Although the displacement pattern seems clear, the mechanisms underlying competitive advantage remain unclear. The ability of ant workers to produce relatively larger amount of alarm pheromone may correspond to relative greater fitness among sympatric fire ant species. Here we report on quantitative intra-specific (i.e. inter-caste) and inter-specific differences of alarm pheromone component, 2-ethyl-3,6-dimethylpyrazine (2E36DMP), for several fire ant species. The alarm pheromone component was extracted by soaking ants in hexane for 48 h and subsequently quantified by gas chromatography-mass spectrometry at single ion monitoring mode. Solenopsis invicta workers had more 2E36DMP than male or female alates by relative weight; individual workers, however, contained significantly less pyrazine. We thus believe that alarm pheromones may serve additional roles in alates. Workers of Solenopsis richteri, S. invicta, and hybrid (S. richteri × S. invicta) had significantly more 2E36DMP than a native fire ant species, Solenopsis geminata. The hybrid fire ant had significantly less 2E36DMP than the two parent species, S. richteri and S. invicta. It seems likely that higher alarm pheromone content may have favored invasion success of exotic fire ants over native species. We discuss the potential role of inter-specific variation in pyrazine content for the relationship between the observed shifts in the spatial distributions of the three exotic fire ant species in southern United States and the displacement of native fire ant species.

Keywords

2-ethyl-3,6-dimethylpyrazinemyrmecologyinvasion successSolenopsis invictaSolenopsis richteriSolenopsis geminata
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 5 , October 2018 , pp. 667 - 673
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

L. Hu, R.R. Balusu, and W.-Q. Zhang contributed equally to this work.

References

Ascunce, M.S., Yang, C.-C., Oakey, J., Calcaterra, L., Wu, W.-J., Shih, C.-J., Goudet, J., Ross, K.G. & Shoemaker, D. (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331, 1066–1068.Google Scholar
Attygalle, A.B. & Morgan, E.D. (1984) Chemicals from the glands of ants. Chemical Society Reviews 13, 245–278.Google Scholar
Blum, M.S. (1969) Alarm pheromones. Annual Review of Entomology 14, 57–80.Google Scholar
Blum, M.S. (1970) The chemical basis of insect sociality. pp. 61–94 in Beroza, M. (Ed.) Chemicals Controlling Insect Behavior. New York, Academic Press.Google Scholar
Blum, M.S. (1985) Alarm pheromone. pp. 194–224 in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive Insect Physiology Biochemistry and Pharmacology. New York, Pergamon Press Inc.Google Scholar
Blum, M.S., Snelling, R.R., Duffield, R.M., Herman, H.R. Jr. & Lloyd, H.A. (1988) Mandibular gland chemistry of Camponotus (Myrmothrix) abdominalis: chemistry and chemosystematic implications (Hymenoptera: Formicidae). pp. 481–490 in Trager, J.C. (Ed.) Advances in Myrmecology. New York, E. Brill Publishing.Google Scholar
Brand, J.M., Duffield, R.M., MacConnell, J.G., Blum, M.S. & Fales, H.M. (1973) Caste-specific compounds in male carpenter ants. Science 179, 388–389.Google Scholar
Buechel, S.D., Wurm, Y. & Keller, L. (2014) Social chromosome variants differentially affect queen determination and the survival of workers in the fire ant Solenopsis invicta. Molecular Ecology 23, 5117–5127.Google Scholar
Buss, L.W. (1981) Group living, competition, and the evolution of cooperation in a sessile invertebrate. Science 213, 1012–1014.Google Scholar
Calabi, P. & Porter, S.D. (1989) Worker longevity in the fire ant Solenopsis invicta: ergonomic considerations of correlations between temperature, size and metabolic rates. Journal of Insect Physiology 35, 643–649.Google Scholar
Callcott, A.-M.A. & Collins, H.L. (1996) Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918–1995. Florida Entomologist 79, 240–251.Google Scholar
Callcott, A.-M.A., Porter, S.D., Weeks, R.D. Jr., Graham, L.C.F., Johnson, S.J. & Gilbert, L.E. (2011) Fire ant decapitating fly cooperative release programs (1994–2008): two Pseudacteon species, P. tricuspis and P. curvatus, rapidly expand across imported fire ant populations in the southeastern United States. Journal of Insect Science 11, 1–25.Google Scholar
Chen, L., Hu, Q.-B. & Fadamiro, H.Y. (2010) Reduction of venom alkaloids in Solenopsis richteri ´ Solenopsis invicta hybrid: an attempt to identify new alkaloidal components. Journal of Agricultural and Food Chemistry 58, 11534–11542.Google Scholar
Choi, M.Y. & Vander Meer, R.K. (2015) Multiple functions of fire ant Solenopsis invicta mandibular gland products. Physiological Entomology 40, 196–204.Google Scholar
Colautti, R.I. & Richardson, D.M. (2009) Subjectivity and flexibility in invasion terminology: too much of a good thing? Biological Invasions 11, 1225–1229.Google Scholar
Diffie, S., Vander Meer, R.K. & Bass, M.H. (1988) Discovery of hybrid fire ant populations in Georgia and Alabama. Journal of Entomological Science 23, 187–191.Google Scholar
Do Nascimento, R.R., Morgan, E.D., Billen, J., Schoeters, E., Della Lucia, T.M.C. & Bento, J.M.S. (1993) Variation with caste of the mandibular gland secretion in the leaf-cutting ant Atta sexdens rubropilosa. Journal of Chemical Ecology 19, 907–918.Google Scholar
Fadamiro, H.Y., He, X.-F. & Chen, L. (2009) Aggression in imported fire ants: an explanation for shifts in their spatial distributions in southern United States? Ecological Entomology 34, 427–436.Google Scholar
Fang, M. & Cadwallader, K.R. (2013) Convenient synthesis of stable deuterium-labeled alkylpyrazines for use in stable isotope dilution assays. Journal of Agricultural and Food Chemistry 61, 3580–3588.Google Scholar
Giraud, T., Pedersen, J.S. & Keller, L. (2002) Evolution of supercolonies: the Argentine ants of Southern Europe. Proceedings of the National Academy of Sciences of the United States of America 99, 6075–6079.Google Scholar
Guan, D., Lu, Y.-Y., Liao, X.-L., Wang, L. & Chen, L. (2014) Electroantennogram and behavioral responses of the imported fire ant, Solenopsis invicta Buren, to an alarm pheromone component and its analogues. Journal of Agricultural and Food Chemistry 62, 11924–11932.Google Scholar
Hernández, J.V., Cabrera, A. & Jaffe, K. (1999) Mandibular gland secretion in different castes of the leaf-cutter ant Atta laevigata. Journal of Chemical Ecology 25, 2433–2444.Google Scholar
Holway, D.A., Lach, L., Suarez, A.V., Tsutsui, N.D. & Case, T.J. (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics 33, 181–233.Google Scholar
Hughes, W.O.H., Howse, P.E. & Goulson, D. (2001) Mandibular gland chemistry of grass-cutting ants: species, caste, and colony variation. Journal of Chemical Ecology 27, 109–124.Google Scholar
Jones, S.R. & Phillips, S.A. (1987) Aggressive and defensive propensities of Solenopsis invicta (Hymenoptera, Formicidae) and 3 indigenous ant species in Texas. Texas Journal of Science 39, 107–115.Google Scholar
Lach, L., Parr, C.L. & Abbott, K.L. (2010) Ant Ecology. Oxford, Oxford University Press.Google Scholar
Lloyd, H.A., Blum, M.S. & Duffield, R.M. (1975) Chemistry of the male mandibular gland secretion of the ant, Camponotus clarithorax. Insect Biochemistry 5, 489–494.Google Scholar
Maschwitz, U.W. (1964) Alarm substances and alarm behaviour in social Hymenoptera. Nature 204, 324–327.Google Scholar
Mizunami, M., Yamagata, N. & Nishino, H. (2010) Alarm pheromone processing in the ant brain: an evolutionary perspective. Frontiers in Behavioral Neuroscience 4, 28.Google Scholar
Morgan, E.D. (2009) Trail pheromones of ants. Physiological Entomology 34, 1–17.Google Scholar
Morrison, L.W. (2000) Mechanisms of interspecific competition among an invasive and two native fire ants. Oikos 90, 238–252.Google Scholar
Obin, M.S. & Vander Meer, R.K. (1989) Between- and within-species recognition among imported fire ants and their hybrids (Hymenoptera: Formicidae): application to hybrid zone dynamics. Annals of the Entomological Society of America 82, 649–652.Google Scholar
Oliver, J.B., Vander Meer, R.K., Ochieng, S.A., Youssef, N.N., Pantaleoni, E., Mrema, F.A., Vail, K.M., Parkman, J.P., Valles, S.M., Haun, W.C. & Powell, S. (2009) Statewide survey of imported fire ant (Hymenoptera: Formicidae) populations in Tennessee. Journal of Entomological Science 44, 149–157.Google Scholar
Pitts, J.P., McHugh, J.V. & Ross, K.G. (2005) Cladistic analysis of the fire ants of the Solenopsis saevissima species-group (Hymenoptera: Formicidae). Zoologica Scripta 34, 493–505.Google Scholar
Porter, S.D. (1992) Frequency and distribution of polygyne fire ants (Hymenoptera: Formicidae) in Florida. Florida Entomologist 75, 248–256.Google Scholar
Porter, S.D. (2000) Host specificity and risk assessment of releasing the decapitating fly Pseudacteon curvatus as a classical biocontrol agent for imported fire ants. Biological Control 19, 35–47.Google Scholar
Showalter, D., Troyer, E., Aklu, M., Jang, E. & Siderhurst, M. (2010) Alkylpyrazines: alarm pheromone components of the little fire ant, Wasmannia auropunctata (Roger) (Hymenoptera, Formicidae). Insectes Sociaux 57, 223–232.Google Scholar
Spigno, G., Tramelli, L. & De Faveri, D.M. (2007) Effects of extraction time, temperature and solvent on concentration and antioxidant activity of grape marc phenolics. Journal of Food Engineering 81, 200–208.Google Scholar
Streett, D.A., Freeland, T.B. Jr. & Vander Meer, R.K. (2006) Survey of imported fire ant (Hymenoptera: Formicidae) populations in Mississippi. Florida Entomologist 89, 91–92.Google Scholar
Sun, Y., Shao, K.-M., Lu, Y.-Y., Shi, Q.-H., Wang, W.-K. & Chen, L. (2017) Electrophysiological and alarm behavioral responses of Solenopsis invicta Buren (Hymenoptera: Formicidae) to alkoxypyrazines. Journal of Asia-Pacific Entomology 20, 541–546.Google Scholar
Tan, M.C., Tan, C.P. & Ho, C.W. (2013) Effects of extraction solvent system, time and temperature on total phenolic content of henna (Lawsonia inermis) stems. International Food Research Journal 20, 3117–3123.Google Scholar
Tschinkel, W.R. (2006) The Fire Ants. Cambridge, Harvard University Press.Google Scholar
Tsutsui, N.D., Suarez, A.V. & Grosberg, R.K. (2003) Genetic diversity, asymmetrical aggression, and recognition in a widespread invasive species. Proceedings of the National Academy of Sciences 100, 1078–1083.Google Scholar
Upadhya, V., Pai, S.R. & Hegde, H.V. (2015) Effect of method and time of extraction on total phenolic content in comparison with antioxidant activities in different parts of Achyranthes aspera. Journal of King Saud University – Science 27, 204–208.Google Scholar
Vander Meer, R.K. & Lofgren, C.S. (1988) Use of chemical characters in defining populations of fire ants, Solenopsis saevissima complex (Hymenoptera: Formicidae). Florida Entomologist 71, 323–332.Google Scholar
Vander Meer, R.K. & Morel, L. (1998) Nestmate recognition in ants. pp. 79–103 in Vander Meer, R.K., Breed, M.D., Espelie, K.E. and Winston, M.L. (Eds) Pheromone Communication in Social Insects. Boulder, Colorado, Westview Press.Google Scholar
Vander Meer, R.K., Preston, C. & Choi, M.-Y. (2010) Isolation of a pyrazine alarm pheromone component from the fire ant, Solenopsis invicta. Journal of Chemical Ecology 36, 163–170.Google Scholar
Wetterer, J.K. (2011) Worldwide spread of the tropical fire ant, Solenopsis geminata (Hymenoptera: Formicidae). Myrmecological News 14, 21–35.Google Scholar
Williamson, M. (1996) Biological Invasions. London, Chapman & Hall.Google Scholar
Wilson, E.O. (1951) Variation and adaptation in the imported fire ant. Evolution 5, 68–79.Google Scholar
Wilson, E.O. (1958) Origin of the variation in the imported fire ant. Evolution 7, 262–263.Google Scholar
Wilson, E.O. (1962) Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith). 1. The organization of mass-foraging. Animal Behaviour 10, 134–147.Google Scholar
Wilson, E.O. (1965) Chemical communication in the social insects. Science 149, 1064–1071.Google Scholar
Wojcik, D.P. (1994) Impact of the red imported fire ant on native ant species in Florida. pp. 269–281 in Williams, D.F. (Ed.) Exotic Ants: Biology, Impact, and Control of Introduced Species. San Francisco, CA, Westview.Google Scholar
Supplementary material: File

Hu et al supplementary material

Table S1

Download Hu et al supplementary material(File)
File 16.2 KB