Communication and Defense in a Pantropical Ant Paratrechina longicornis
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
Characteristics of Invasive
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.
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).
Invasive ants are of comparable small body size which
enables a larger population number at a given energy input (McGlynn,
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).
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
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.
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
Exploitative and Interference
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.
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.
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.
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
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.
Dr. Jerrold Meinwald, Chemistry and Chemical Biology, Cornell University,
Dr. Athula Attygalle, Chemistry and Chemical Biology, Stevens Institute
of Technology, Hoboken, NJ
Leif Abrell, Chemistry Unit, Biosphere 2 Research, Columbia University,
New York, NY
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
Davidson, D. W., 1998. Resource discovery
vesus resource domination in ants: a functional mechanism for breaking
the trade-off. Ecol. Entomol. 23: 484-490.
Fluker, S. S. and J. W. Beardsley, 1970.
Sympatric associations of three ants: Iridomyrmex humilis, Pheidole
megacephala, and Anoplolepis longipes in Hawaii. Ann. Entomol.
Soc. Am. 63: 1290-96.
Giraud, T., J. S. Pedersen and L. Keller,
2002. Evolution of supercolonies: The Argentine ants of southern Europe.
PNAS 99: 6075-6079.
Holway, D. and T. Case, 2000. Mechanisms
of dispersed central-place foraging in polydomous colonies of the Argentine
ant. Anim Behav 59: 433-441.
Holway, D. A., L. Lach, A. V. Suarez, N.
D. Tsutsui and T. J. Case, 2002. The causes and consequences of ant
invasions. Annu. Rev. Ecol. Syst. 33: 181-233.
Holway, D. A. and A. V. Suarez, 1999. Animal
behavior: an essential component of invasion biology. Trends Ecol. Evol.
Holway, D. A., A. V. Suarez and T. J. Case,
1998. Loss of intraspecific aggression in the success of a widespread
invasive social insect. Science 282: 949-952.
Human, K. G. and D. M. Gordon, 1996. Exploitation
and interference competition between the invasive Argentine ant, Linepithema
humile, and native ant species. Oecologia 105: 405-412.
McGlynn, T. P., 1999. Non-native ants are
smaller than related native ants. Am. Nat. 154: 690-699. Passera, L.,
1994. Characteristics of tramp species. In: Exotic ants: Biology, impact,
and control of introduced species (D. F. Williams, Ed.), Westview Press,
Boulder, Colorado, USA. pp. 23-43.
Ross, K. G., E. L. Vargo and L. Keller,
1996. Social evolution in a new environment: the case of introduced
fire ants. Proc. Natl. Acad. Sci. U.S.A. 93: 3021-3025.
Trager, J. C., 1984. A revision of the
genus Paratrechina (Hymenoptera: Formicidae) of the continental
United States. Sociobiology 9: 49-162.
Tsutsui, N. D. and T. J. Case, 2001. Population
genetics and colony structure of the argentine ant (Linepithema humile)
in its native and introduced range. Evolution 55: 976-985.
Tsutsui, N. D., A. V. Suarez, D. A. Holway
and T. J. Case, 2000. Reduced genetic variation and success of an invasive
species. PNAS 97: 5948-5953.
Wetterer, J. K., C. Dunning, M. Yospin
and A. Himler, 1997. Invertebrate diversity and ecology in Biosphere
2. Pages 119-122. Invertebrates in captivity Conference Proceedings.
Sonoran Arthropod Studies Institute, Tuscon, AZ, USA.
Wetterer, J. K., S. E. Miller, D. E. Wheeler,
C. A. Olson, D. A. Polhemus, M. Pitts, I. W. Ashton, A. G. Himler, M.
M. Yospin, K. R. Helms, E. L. Harken, J. Gallaher, C. E. Dunning, M.
Nelson, J. Litsinger, A. Southern and T. L. Burgess, 1999. Ecological
dominance by Paratrechina longicornis (Hymenoptera: Formicidae),
an invasive tramp ant, in Biosphere 2. Florida Entomol. 82: 381-388.