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Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)

SIMPLE SUMMARY: Grooming is a common behavior in animals. It serves the function of removing foreign materials and excessive amounts of self-secreted materials from the body’s surface. Social insects, such as honeybees or ants, use various types of pheromones, some of which propagate information abo...

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Autores principales: Mizutani, Hitomi, Tagai, Kazuhiro, Habe, Shunya, Takaku, Yasuharu, Uebi, Tatsuya, Kimura, Toshifumi, Hariyama, Takahiko, Ozaki, Mamiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8471180/
https://www.ncbi.nlm.nih.gov/pubmed/34564213
http://dx.doi.org/10.3390/insects12090773
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author Mizutani, Hitomi
Tagai, Kazuhiro
Habe, Shunya
Takaku, Yasuharu
Uebi, Tatsuya
Kimura, Toshifumi
Hariyama, Takahiko
Ozaki, Mamiko
author_facet Mizutani, Hitomi
Tagai, Kazuhiro
Habe, Shunya
Takaku, Yasuharu
Uebi, Tatsuya
Kimura, Toshifumi
Hariyama, Takahiko
Ozaki, Mamiko
author_sort Mizutani, Hitomi
collection PubMed
description SIMPLE SUMMARY: Grooming is a common behavior in animals. It serves the function of removing foreign materials and excessive amounts of self-secreted materials from the body’s surface. Social insects, such as honeybees or ants, use various types of pheromones, some of which propagate information about the environment to conspecific individuals, for chemical communication. The individuals that receive such information can respond with suitable behaviors to protect themselves and their society. Hence, grooming is important for the maintenance of the correct performance of their sensory organs on antennae for pheromone perception. Here, we experimentally limited self-grooming of the antennae in workers of the Japanese carpenter ant (Camponotus japonicus) by removing a pair of antennal cleaning apparatuses from the forelegs and investigated their behavioral change in response to exposure to the alarm pheromone or to encounters with nestmates or non-nestmates. Comparisons between self-grooming-nonlimited and self-grooming-limited ants showed that the self-grooming-limited ants gradually exhibited decreased locomotion activity in their fight-or-flight response to the alarm pheromone and experienced increased failure in nestmate and non-nestmate discrimination. Thus, the results of the present study suggest that antennal sensory system maintenance supports social communication, which is indispensable not only to the individual workers but also to the survival of their society. ABSTRACT: Self-grooming of the antennae is frequently observed in ants. This antennal maintenance behavior is presumed to be essential for effective chemical communication but, to our knowledge, this has not yet been well studied. When we removed the antenna-cleaning apparatuses of the Japanese carpenter ant (C. japonicus) to limit the self-grooming of the antennae, the worker ants demonstrated the self-grooming gesture as usual, but the antennal surface could not be sufficiently cleaned. By using scanning electron microscopy with NanoSuit, we observed the ants’ antennae for up to 48 h and found that the antennal surfaces gradually became covered with self-secreted surface material. Concurrently, the self-grooming-limited workers gradually lost their behavioral responsiveness to undecane—the alarm pheromone. Indeed, their locomotive response to the alarm pheromone diminished for up to 24 h after the antenna cleaner removal operation. In addition, the self-grooming-limited workers exhibited less frequent aggressive behavior toward non-nestmate workers, and 36 h after the operation, approximately half of the encountered non-nestmate workers were accepted as nestmates. These results suggest that the antennal sensing system is affected by excess surface material; hence, their proper function is prevented until they are cleaned.
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spelling pubmed-84711802021-09-27 Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus) Mizutani, Hitomi Tagai, Kazuhiro Habe, Shunya Takaku, Yasuharu Uebi, Tatsuya Kimura, Toshifumi Hariyama, Takahiko Ozaki, Mamiko Insects Article SIMPLE SUMMARY: Grooming is a common behavior in animals. It serves the function of removing foreign materials and excessive amounts of self-secreted materials from the body’s surface. Social insects, such as honeybees or ants, use various types of pheromones, some of which propagate information about the environment to conspecific individuals, for chemical communication. The individuals that receive such information can respond with suitable behaviors to protect themselves and their society. Hence, grooming is important for the maintenance of the correct performance of their sensory organs on antennae for pheromone perception. Here, we experimentally limited self-grooming of the antennae in workers of the Japanese carpenter ant (Camponotus japonicus) by removing a pair of antennal cleaning apparatuses from the forelegs and investigated their behavioral change in response to exposure to the alarm pheromone or to encounters with nestmates or non-nestmates. Comparisons between self-grooming-nonlimited and self-grooming-limited ants showed that the self-grooming-limited ants gradually exhibited decreased locomotion activity in their fight-or-flight response to the alarm pheromone and experienced increased failure in nestmate and non-nestmate discrimination. Thus, the results of the present study suggest that antennal sensory system maintenance supports social communication, which is indispensable not only to the individual workers but also to the survival of their society. ABSTRACT: Self-grooming of the antennae is frequently observed in ants. This antennal maintenance behavior is presumed to be essential for effective chemical communication but, to our knowledge, this has not yet been well studied. When we removed the antenna-cleaning apparatuses of the Japanese carpenter ant (C. japonicus) to limit the self-grooming of the antennae, the worker ants demonstrated the self-grooming gesture as usual, but the antennal surface could not be sufficiently cleaned. By using scanning electron microscopy with NanoSuit, we observed the ants’ antennae for up to 48 h and found that the antennal surfaces gradually became covered with self-secreted surface material. Concurrently, the self-grooming-limited workers gradually lost their behavioral responsiveness to undecane—the alarm pheromone. Indeed, their locomotive response to the alarm pheromone diminished for up to 24 h after the antenna cleaner removal operation. In addition, the self-grooming-limited workers exhibited less frequent aggressive behavior toward non-nestmate workers, and 36 h after the operation, approximately half of the encountered non-nestmate workers were accepted as nestmates. These results suggest that the antennal sensing system is affected by excess surface material; hence, their proper function is prevented until they are cleaned. MDPI 2021-08-28 /pmc/articles/PMC8471180/ /pubmed/34564213 http://dx.doi.org/10.3390/insects12090773 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Mizutani, Hitomi
Tagai, Kazuhiro
Habe, Shunya
Takaku, Yasuharu
Uebi, Tatsuya
Kimura, Toshifumi
Hariyama, Takahiko
Ozaki, Mamiko
Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title_full Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title_fullStr Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title_full_unstemmed Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title_short Antenna Cleaning Is Essential for Precise Behavioral Response to Alarm Pheromone and Nestmate–Non-Nestmate Discrimination in Japanese Carpenter Ants (Camponotus japonicus)
title_sort antenna cleaning is essential for precise behavioral response to alarm pheromone and nestmate–non-nestmate discrimination in japanese carpenter ants (camponotus japonicus)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8471180/
https://www.ncbi.nlm.nih.gov/pubmed/34564213
http://dx.doi.org/10.3390/insects12090773
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