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Characteristic behavior of the Japanese carpenter ant


Mamiko Ozaki(Kobe University)


The behavior and life style of a eusocial insect


Eusocial insects have the following characteristics: (1) cooperative brood care of the offspring from multiple conspecific individuals, (2) overlapping generations of adults within a society which is often called colony, and (3) existence of individuals who reproduce (reproductive caste) and those who do not reproduce (infertile caste) and divisions of labor as specialized behavioral groups. These lifestyle patterns are essential factors for definition of eusociality. The Japanese carpenter ant is a typical example of eusocial insects. Several generations of ants of the same species live together in the same colony, and the fertile and infertile castes cooperate in maintaining and/or developing own colony. Colony formation starts by a single mated queen on mild afternoons around the monsoon season in Japan, when temperature and humidity are relatively high. The virgin queens and male ants simultaneously fly off all together from neighboring nests for the wedding flight (Fig. 1), during which they mate in the air. The queens who land safely on the ground drop their wings and start a new colony by preparing a nest and laying eggs.

   


Fig. 1 The wedding flight is assisted by worker ants, a winged male on the far side of the nest and the virgin queens with a large head on the near side of the nest are peering out.
(Provider:Masachika Ishimura, Kobe University))


In each colony of the carpenter ant, there is only one queen who has the role of reproducing. The other individuals in the colony are workers, males, and next generation queens (virgin queens). The colony is a social unit bound together with kinship ties. In order to establish and maintain the colony, individuals need a mechanism to distinguish between colony members and outsiders and to switch behavior patterns appropriately; this is particularly necessary for forager worker ants.

Different roles of worker ants may be determined by age. Young workers look after the queen, next generation queens, males, eggs, and larvae. As worker ants grow older, they venture outside the nest for foraging duties. They cooperate in foraging, which is moving in a characteristic small procession known as the “tandem march” (Fig. 2). A worker who finds a food source selects a short-cutting route back to the nest, recruits several worker ants (followers), and guides them to the food source as a leader. This helps improve the efficiency of foraging. Recruiting and leading the followers are believed to be achieved by a pheromonal signal, the mechanism of which has not been fully elucidated. The leader and follower roles are not predetermined. The individual who returned to the nest with information of the food source, goes back to the food source as the leader, relying on visual cues and associated memory to find the food source, while secretes an unidentified volatile pheromone from its tail end. The followers use olfactory cues from the pheromone to enable them to follow the leader. Because the march consisting of a leader and the followers falls apart when the distance between them becomes so long that the pheromone cold not maintain the followers’ attention, the followers look to remain neither too close to nor too distant from the leader during marching. Ants utilize various pheromones or signature chemicals for enhancing cooperativity among nestmetes within a colony and rejecting conspecific non-nestmates and hetrospecifics.





Fig. 2: The tandem march: the followers follow the chemical signal of the leader
(Provider: Masaru Hojo ,University of the Ryukyus)



Nestmate recognition behavior

In a monogyne society, such as that of the Japanese carpenter ant, the terms of “nest” and “colony” may be used as the same entity. Nestmate recognition is essential for their decision making of aggressive behavior toward other colony members regardless of con- or heterospcifics or sometimes escaping behavior. When worker ants encounter each other (Fig. 3A), they first investigate each other with their antennae, which have olfactory organs (antennation; Fig. 3B). If one recognizes that the other is not a nest mate, they will attack her to reject. Aggressive behavior of ants appears stepwise; mandible opening, biting (Fig, 3C) , splaying formic acid from the tail end (Fig. 3D). Such a nestmate recognition is based on match/mismatch of odors of their body surface materials.


      


Fig. 3: When ants belonging to different nests encounter each other, they show aggressive behavior after antennation.
(Provider: Midori Kobayashi, Kobe University)



Cuticular hydrocarbons (CHCs) of the Japanese carpenter ant consists of 18 non-volatile, water-insoluble components. The mixing ratio of these CHCs is colony-specific and is common to the worker ants within a colony (Fig. 4). From a chemical ecology standpoint, the odor of CHCs have been suggested to play the key role in nestmate recognition of ants.


      

Fig. 4: An comparison of gas chromatograms of CHCs of worker ants from different nests [adapted from Ozaki et al., Science (2005)]


In addition, it has been shown that the basiconic sensilla on the surface of the worker antennae to CHCs respond in the Japanese carpenter ants (Fig. 5). These basiconic sensilla do not respond to nestmate CHCs but non-nestmate CHCs, regardless of the mixing ratios. (Fig.6)(Ozaki et al., 2005)

      

Fig. 5: Hydrocarbon-sensitive basiconic sensilla on the antenna of a worker of the Japanese carpenter ant
(Provider: Masayuki Iwasaki, Fukuoka University)



The behavioral switching based on nestmate recognition is begun with olfactory discrimination between nestmates and non-nestmate, which may be explained at the sensory organ level, because the aggressive behavior is believed to be triggered by the response of the basiconic sensilla. An important feature of the nestmate recognition system is that the basiconic sensilla, when stimulated with the cuticular hydrocarbons of a nestmate, keep silent (Fig. 6). The putative explanation is that the basiconic sensilla are desensitized to stimulation with the nestmate CHC pattern identical to the own CHC pattern. Another aspect of CHC pattern recognition is a peri-receptor mechanism by which the hydrophilic environment surrounding the receptor membranes of olfactory receptor neurons (ORNs) inside the basiconic sensilla dissolve those water-insoluble CHCs. It is achieved with the help of chemosensory protein (CSP), which is secreted into the receptor lymph inside the basiconic sensilla, binds the CHCs and transports them to the receptor membrane surfaces of the ORNs, keeping the original composition of the CHCs. (Fig.7,8)(Ozaki et al., 2005)。

 

Fig. 6: Basiconic sensilla response
They respond to non-nestmate CHCs but not to nestmate CHCs. [adapted from Ozaki et al., Science (2005)]



Fig. 7: Solubilization of CHCs with the help of CSP: Transfer into a hydrophilic environment, maintaining the compositional ratio.
[adapted from Ozaki et al., Science (2005)]


Fig. 8: Model of peri-receptor events in the basiconic sensilla of worker ants; transport and reception of CHCs mediated by CSP.
(Provider: Ayako Katsumata, University of North Carolina)



In a polygyne society of supercolony-forming species, the terms of “nest” and “colony” cannot be used as the same entity. In these species, workers from nearby nests can freely move between the nests. In this case, the integrated nest as a whole can be regarded as a colony referred to as a supercolony. In the Japanese red wood ants (Formica yessensis), which build this type of supercolony consisting of multiple nests, the similar CHCs within a supercolony is the key for the behavioral switching between acceptance and rejection, regardless of degree of kinship (Kidokoro-Kobayashi et al., 2012). The Argentine ant (Linepithema humile) originated in South America, has invaded all over the world and constructs world-wide huge super colonies by combining nests. Also in this ant, the CHCs are believed to be the key (Torres et al., 2007), although it has recently been suggested that other body surface substances are also involved in colonymate recognition.

Symbiosis between ants and lycaenid butterflies


There are several ant species that take care of lycaenid caterpillars. Mother butterfly of Niphanda fusca chooses the nesting and/or foraging places of the host ants, Camponotus japonicus, for her egg laying sites. The worker ants take the second instar caterpillars to the nest, feed, and clean them. When the caterpillars have been reared to the final instar, they move to the nest entrance and pupate there. This is supposedly because the adult butterflies may be treated as food by the ants and attacked; therefore, this strategy allows the enclosed adult to immediately move away from the ant nest. Nevertheless, the caterpillars and pupae of Niphanda fusca are not attacked by the Japanese carpenter ants, but are looked after by the workers. Concerned with this phenomenon, two types of chemical trick are known; First, the caterpillars secrete honey dew cocktail containing trehalose and glycine, taste of which is adapted to the host ant-specific preference (Fig. 9; Hojo et al., 2008). Second, the lycaenid caterpillars chemically mimic the CHC odor of males of the host ant species. Since the reproductive caste is given special attention by the workers, this chemical trick is a good strategy for the caterpillars to get special care.
(Fig.10)(Hojo et al., 2009)




Fig. 9: Honey dew secretions of the Japanese carpenter ant. The Japanese carpenter ant favors a cocktail of trehalose
and glycine (Top: taste receptor neuron activity in an ant; Bottom: ant licking the honeydew)
[adapted from Hojo et al., J Comp Physiol A (2008)
Photo provider: Masaru Houjyou, Universith of the Ryukyus]





Fig. 10: Chemical mimicry in a species of Lycaenidae, Niphanda fusca by resembling hydrocarbons of males of Japanese carpenter ant, Camponotus japonicus. [adapted from Hojo et al., Proc Roy Soc B(2009)]


References


Hojo M, Wada-Katsumata A, Ozaki M, Yamaguchi S, Yamaoka R (2008) Gustatory synergism in ants mediates a species-specific symbiosis with lycaenid butterflies.J Comp Physiol A 194:1043-1052.

Hojo M, Wada-Katsumata A, Akino T, Yamaguchi S, Ozaki M, Yamaoka R (2009) Chemical disguise as particular caste of host ants in the inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae). Proc Roy Soc B 276:551-558.

Kidokoro-Kobayashi M, Iwakura M, Fujiwara-Tsujii N, Fujiwara S, Sakura M, Sakamoto H, Higashi S, Hefetz A, Ozaki M (2012) Chemical discrimination and aggressiveness via cuticular hydrocarbons in a supercolony-forming ant, Formica yessensis. PLOS ONE 7:e46840.

Ozaki M, Wada-Katsumata A, Fujikawa N, Iwasaki M, Yokohari F, Satoji Y, T, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311-314.

Torres C W, Brandt M, Tsutsui N D (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insect Soc 54:363–373.

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