Chemical identification of an active component and putative neural mechanism for repellent effect of a native ant’s odor on invasive species

The invasive Argentine ants (Linepithema humile) and the red imported fire ants (Solenopsis invicta) constitute a worldwide threat, causing severe disruption to ecological systems and harming human welfare. In view of the limited success of current pest control measures, we propose here to employ repellents as means to mitigate the effect of these species. We demonstrate that cuticular hydrocarbons (CHCs) used as nestmate-recognition pheromone in the Japanese carpenter ant (Camponotus japonicus), and particularly its (Z)-9-tricosene component, induced vigorous olfactory response and intense aversion in these invasive species. (Z)-9-Tricosene, when given to their antennae, caused indiscriminate glomerular activation of antennal lobe (AL) regions, creating neural disarray and leading to aversive behavior. Considering the putative massive central neural effect, we suggest that the appropriate use of certain CHCs of native ants can facilitate aversive withdrawal of invasive ants.

[1]  M. Ozaki,et al.  Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus) , 2021, Insects.

[2]  M. Ozaki,et al.  Visualization of antennal lobe glomeruli activated by nonappetitive D-limonene and appetitive 1-octen-3-ol odors via two types of olfactory organs in the blowfly Phormia regina , 2020, Zoological letters.

[3]  Toshiaki Omori,et al.  Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation , 2018, Front. Cell. Neurosci..

[4]  K. Goka,et al.  Declaration of local chemical eradication of the Argentine ant: Bayesian estimation with a multinomial-mixture model , 2017, Scientific Reports.

[5]  S. Higashi,et al.  Relationship Among Establishment Durations, Kin Relatedness, Aggressiveness, and Distance Between Populations of Eight Invasive Argentine Ant (Hymenoptera: Formicidae) Supercolonies in Japan , 2017, Journal of Economic Entomology.

[6]  S. Reitz,et al.  Emerging Themes in Our Understanding of Species Displacements. , 2017, Annual review of entomology.

[7]  K. Goka,et al.  Surveys of the ant faunas at ports of Tokyo Bay and the Ogasawara Islands , 2016, Applied Entomology and Zoology.

[8]  M. Ohkura,et al.  Olfactory receptor for prostaglandin F2α mediates male fish courtship behavior , 2016, Nature Neuroscience.

[9]  P. Lester,et al.  Synthetic pheromones as a management technique - dispensers reduce Linepithema humile activity in a commercial vineyard. , 2016, Pest management science.

[10]  Matt Ziegler,et al.  Visualizing and interacting with large-volume biodiversity data using client-server web-mapping applications: The design and implementation of antmaps.org , 2016, Ecol. Informatics.

[11]  S. Shigenobu,et al.  Antennal RNA-sequencing analysis reveals evolutionary aspects of chemosensory proteins in the carpenter ant, Camponotus japonicus , 2015, Scientific Reports.

[12]  Anandasankar Ray,et al.  Cuticular Hydrocarbon Pheromones for Social Behavior and Their Coding in the Ant Antenna. , 2015, Cell reports.

[13]  K. Goka,et al.  Ecological impacts on native ant and ground-dwelling animal communities through Argentine ant (Linepithema humile) (Hymenoptera: Formicidae) management in Japan , 2015, Applied Entomology and Zoology.

[14]  J. Millar,et al.  Isolation and determination of absolute configurations of insect-produced methyl-branched hydrocarbons , 2015, Proceedings of the National Academy of Sciences.

[15]  A. Hefetz,et al.  Neural Mechanisms and Information Processing in Recognition Systems , 2014, Insects.

[16]  M. Nishikawa,et al.  Higher brain centers for social tasks in worker ants, Camponotus japonicus , 2012, The Journal of comparative neurology.

[17]  P. d’Ettorre,et al.  Recognition of Social Identity in Ants , 2012, Front. Psychology.

[18]  W. Rössler,et al.  Friends and Foes from an Ant Brain's Point of View – Neuronal Correlates of Colony Odors in a Social Insect , 2011, PloS one.

[19]  Natasha P. Mothapo,et al.  Behavioural and chemical evidence for multiple colonisation of the Argentine ant, Linepithema humile, in the Western Cape, South Africa , 2011, BMC Ecology.

[20]  D. O'dowd,et al.  Genetic structure, behaviour and invasion history of the Argentine ant supercolony in Australia , 2010, Evolutionary applications.

[21]  H. Nishino,et al.  Sex‐specific antennal sensory system in the ant Camponotus japonicus: Glomerular organizations of antennal lobes , 2010, The Journal of comparative neurology.

[22]  N. Tsutsui,et al.  The global expansion of a single ant supercolony , 2010, Evolutionary applications.

[23]  C. Green,et al.  Twenty years of Argentine ants in New Zealand: past research and future priorities for applied management , 2010 .

[24]  J. Silverman,et al.  Effect of an Invasive and Native Ant on a Field Population of the Black Citrus Aphid (Hemiptera: Aphididae) , 2009, Environmental entomology.

[25]  Wolfgang Rössler,et al.  Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. , 2008, Arthropod structure & development.

[26]  Wolfgang Rössler,et al.  Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus , 2008, The Journal of comparative neurology.

[27]  R. Yamaoka,et al.  Ant Nestmate and Non-Nestmate Discrimination by a Chemosensory Sensillum , 2005, Science.

[28]  L. Keller,et al.  Evolution of supercolonies: The Argentine ants of southern Europe , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Suarez,et al.  BOTTOM-UP EFFECTS ON PERSISTENCE OF A SPECIALIST PREDATOR: ANT INVASIONS AND HORNED LIZARDS , 2002 .

[30]  A. Suarez,et al.  Reduced genetic variation and the success of an invasive species. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Gordon,et al.  Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species , 1996, Oecologia.

[32]  C. Sih,et al.  Bifunctional chiral synthons via biochemical methods. III. Optical purity enhancement in enzymic asymmetric catalysis , 1984 .

[33]  Davidr . Evans,et al.  Asymmetric alkylation reactions of chiral imide enolates. A practical approach to the enantioselective synthesis of .alpha.-substituted carboxylic acid derivatives , 1982 .

[34]  E. Wilson,et al.  Chemical Communication and "Propaganda" in Slave-Maker Ants , 1971, Science.

[35]  M. Blum.  Chemical Releasers of Social Behavior. VIII. Citral in the Mandibular Gland Secretion of Lestrimelitta limao (Hymenoptera: Apoidea: Melittidae) , 1966 .

[36]  T. Blackburn,et al.  Displacement and Local Extinction of Native and Endemic Species , 2017 .

[37]  M. Ozaki,et al.  Cuticular hydrocarbon sensillum for nestmate recognition in ants , 2012 .

[38]  G. J. Blomquist.  Insect Hydrocarbons: Biosynthesis of cuticular hydrocarbons , 2010 .

[39]  J. Silverman,et al.  The Argentine ant: challenges in managing an invasive unicolonial pest. , 2008, Annual review of entomology.

[40]  Issg.  100 of the World’s Worst Invasive Alien Species: A Selection From The Global Invasive Species Database , 2000 .

[41]  J. Clément,et al.  Nestmate recognition: the role of cuticular hydrocarbons in the ant Camponotus vagus Scop. , 1987 .

[42]  M. Blum,et al.  Alkylpyrazine alarm pheromones in primitive ants with small colonial units. , 1976, Comparative biochemistry and physiology. B, Comparative biochemistry.