Chemical Communication and Defense in a Pantropical Ant Paratrechina longicornis (Formicidae: Formicinae)

Abstract

Both highly efficient resource utilization and numerical dominance at interference sites are known to be of particular importance for the success of invasive ants. Both traits are based on highly collective behavior which is coordinated mainly by chemical communication. The ecological dominance of the crazy ant P. longicornis can be explained on the basis of its collective skills due to mass communication. The pheromone system of this ant was found to be of extraordinary complexity. Three glands are involved in trail communication. A long lasting (ca. 24 h) orientation pheromone originates from the rectum. This is probably used for stable trunk trails and eventually for territorial marking. A medium lasting (< 1 h) attractant from the poison gland acts as a marker of feeding sites and eventually also in trail recruitment with medium priority. An extremely short lasting (ca. 2 min) pheromone originates from the Dufour gland. This secretion is responsible for extraordinarily fast and efficient recruitment, and provides temporal flexibility of the trail system. The chemical communication system realized in P. longicornis is exceptional among the Formicinae and outstanding within the Formicidae. The significance of such an efficient multi-signal communication system is discussed in regard to competitiveness and invasion success

 

Characteristics of Invasive Ants

Among more than 11 000 ant species currently described, there are a few species of different subfamilies which are extraordinarily successful on a global scale. The so called invasive ants are able to establish themselves in new habitats after being (accidentally) introduced (by humans), thrive and exclude most of the native ant fauna after reaching extraordinary abundance and population density. The ecological impact of invasive species can be dramatic, altering entire communities up to complete displacement of native species, including other animals than ants (Holway et al., 2002). Due to their massive abundance in conjunction with the characteristic to tend homopterans, invasive ants can be even harmful to the local flora. It is of great ecological and economical interest to study the mechanisms which enable these ants to become dominant. Several characteristic traits of invasive ants (listed below) have already been recognized for supporting ecological dominance, however different species certainly rely more or less on the one or other of these strategies.

Nesting Behavior

Invasive ants have generalistic nesting habits and they quickly found new nests as soon as they find suitable locations. For this reason, they are likely to be dispersed by human commerce (therefore the name Tramp Ants) (Passera, 1994).

Body Size

Invasive ants are of comparable small body size which enables a larger population number at a given energy input (McGlynn, 1999).

Colony Structure

Invasive ants are polygyne (multiple queens per nest) and polydome (multiple nests per colony). In fact there are often no clear colony boundaries like commonly found in other ants. For this reason, invasive ants cooperate on a higher level widely without intaspecific competition between colonies. They are often referred to as "unicolonial" although I prefer the term "supercolonial" since there are always colony boundaries, even if these can be extremely wide. The largest known "supercolony" is formed by the Argentine ant Linepithema humile along the northern coast of the Mediterranean sea expanding over 6000 km (Giraud et al., 2002). However, most supercolonies are much smaller. The presence of multiple queens which most likely contribute different gene pools leads to the next point. The supercolony structure supports ecological dominance because of high ant densities and short distances between nests and feeding/interference sites (Holway and Case, 2000; Holway et al., 1998).

Population Genetics

This field has not been very well studied so far. Data is available on the L. humile and S. invicta (Ross et al., 1996; Tsutsui and Case, 2001; Tsutsui et al., 2000). Invasive ants seem to have experienced a loss of genetic variety due to genetic drift at the introduction event (bottleneck hypothesis). This would mean that they are closer related to each other than native populations of the same species. Nevertheless, it remains a mystery how they are able to maintain their extensive supercolonies over time.

Aggression and Defense Behavior

Some invasive ants are known to be extraordinary aggressive (Pheidole megacephala) (Fluker and Beardsley, 1970) or they make use of potent defensive chemicals (typical for Dolichoderinae). However, interestingly, not all species behave aggressive so that does not seem to be a general trait.

Exploitative and Interference Behavior

Exploitative and interference abilities are very well recognized for being crucial in interspecific competition of ants (Davidson, 1998; Holway and Suarez, 1999; Human and Gordon, 1996). Invasive ants are usually faster in locating food and superior in monopolizing resources compared to local species. This can be the case even if the invasive ants do not behave extraordinarily aggressive. Main reason seem to be a numerical advantage at food or interference sites. This leads to the point where my research is settled, the chemical communication.

Chemical Communication

Exploitative and interference behavior are highly collective tasks. Collective behavior in ants is mainly coordinated by chemical cues (pheromones). Activities outside the nest are mainly coordinated by so called trail pheromones which are applied to the substrate and provide information for nestmates such as orientation cues to the nest or information about newly discovered food sources or interference sites. The more sophisticated such a communication is, the more efficient should a species theoretically be in performing these tasks. However, chemical communication in invasive ants is not very well studied. Although some species have been studied to a certain extent, there are still many important species where virtually nothing is known about their trail communication (Monomorium floricola, Solenopsis geminata, Anoplolepis longipes, Wasmannia auropunctata, Tapinoma melanocephalum and Pheidole megacephala).

 

The Crazy Ant

Actually, there are two ant species referred to as "crazy ants", the "long legged" Anoplolepis longipes and the "long horned" Paratrechina longicornis. The latter is the one I work with. P. longicornis is of old world origin (related to Lasius), however, it is distributed worldwide since long times mainly in the tropics and in greenhouses or other structures in the northern hemisphere (Trager, 1984). It has also established itself in the Biosphere 2 Center, a 3.15 acre enclosed and controlled environment facility in Oracle/Arizona. The colonization history of Bio 2 illustrates most dramatically the impact of an ant invasion. 11 ant species were originally introduced together with a variety of other animal and plant species. Three years later, none of these ants could be found (Wetterer et al., 1999). They were replaced by a number of accidentally introduced tramp ants. Finally, after six years, one species, P. longicornis, was by far the most dominant ant in B2, with more than 99.9% abundance (Wetterer et al., 1997). Most arthropods also disappeared during the "takeover" of P. longicornis.

 

Main Results of my Research

Exploitative and Interference Behavior

In competition experiments with two sympatric tramp ants (M. floricola and T. melanocephalum), the crazy ant was faster in locating baits and in recruiting colonymates. Furthermore, it was able to displace competing ants from baits by quick recruitment and numerical dominance without physical aggressiveness. In one by one interactions, it was inferior to the sympatric species since these make use of potent defensive chemistry. The same was observed in interference with the native Forelius pruinosus, which even killed numerous P. longicornis workers at an event when it entered a part of Bio 2. F. pruinosus (as a Dolichoderine) is also known to posses potent defensives. In summary, the dominance of P. longicornis seem to be due to its numerical dominance in exploitation and interference rather than to combative abilities.

Chemical Communication

The pheromone communication of P. longicornis turned out to be rather complex. Typical for fomicines, the rectum was previously known to contain a trail pheromone in P. longicornis too, however, I was able to locate two additional pheromone glands, the Dufor gland and the poison gland. What are the functions of all these glands? The pheromone originating from the rectum has a long persistence of more than 24 h and a strong orientation effect. It is, therefore, most likely used for stable trails and eventually for territorial marking. The poison gland pheromone attracts more ants on a short term and causes accumulation of ants. It is most likely used as a food marker and eventually for medium lasting trails. The Dufour gland pheromone elicits a significant excitement and acceleration in velocity which lasts only about 2 minutes and only a low orientation effect. Such a strong short lasting effect is typical for recruitment pheromones. This pheromone causes the erratic movements which these ants earned their name for.

Discussion

A pheromone system including three components is rather outstanding among the Formicidae and exceptional among the Formicinae. What is the advantage of such a system? Long lasting trails are used to explore permanent food sources like Homopterans. Trophobiosis is in fact an integral part of the crazy ants lifestyle and a typical trait of invasive ants in general. However, long lasting trails contradict with the observed flexibility to switch within minutes to newly discovered food sources. This flexibility is achieved by use of the strong short term pheromone from the Dufour gland. If necessary, numerous ants can be recruited quickly too food or interference sites, as described above, a success strategy in the ecology of P. longicornis. The role of the poison gland is not absolutely clear. It might act as a pheromone with intermediate priority between rectum and Dufour gland, making the communication system better adjustable to environmental cues. It might act synergistically with Dufour gland to enhance recruitment. It is also conceivable, that a distinction between food recruitment and recruitment to interference sites exist. In this case, poison gland and Dufour gland secretion could be used as distinct signals or they could act synergistically in one context. Since it causes accumulation, it appears most likely to me that is a synergist. In conclusion the communication system of P. longicornis clearly supports its ecological dominance. This is probably of special importance after the introduction of a colony fragment into a new area, because at this stage, the most likely small propagule has to compete with local ant species without any numerical advantage due to supercolony structure. Quick mobilization of workers due to sophisticated communication, however, can cause numerical dominance at feeding and interference sites on a spatiotemporal basis. This might help monopolizing resources and enabling final growth of a supercolony.

 

Chemical Characterization of Pheromones

The next step after localization of pheromone sources and studying their biological meaning is the chemical analysis of bioactive gland contents. I am currently involved in the analysis of the crazy ants trail pheromones. Methods I apply in this study are:

Preparation of solvent gland extracts and injection in a preparative gas chromatograph (GC) or different gas chromatographs combined with mass spectrometers (GC/MS). The instruments I use are a HP 5890 GC/MS and a Micromass 6890 GC/MS-TOF (time of flight), capable of chemical and electron ionization (CI and EI) and accurate mass detection.

Preparation of solid samples, sealed in glass capillaries, and injection into a HP 5890 GC/MS with a special solid sample device.

Preparation of samples using solid-phase microextraction (SPME) (headspace or direct contact with dissected glands) and injection into a HP 5890 GC/MS or a Micromass 6890 GC/MS-TOF.

 

Collaborators

Prof. Dr. Jerrold Meinwald, Chemistry and Chemical Biology, Cornell University, Ithaca, NY

Prof. Dr. Athula Attygalle, Chemistry and Chemical Biology, Stevens Institute of Technology, Hoboken, NJ

Dr. Leif Abrell, Chemistry Unit, Biosphere 2 Research, Columbia University, New York, NY

 

Acknowledgements

I am grateful for financial support from the Alexander von Humboldt Foundation (Feodor-Lynen Program) and for a Chemistry Biosphere 2 Program grant from Columbia University.

 

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