PsycheVolume 2012 (2012), Article ID 694910, 11 pagesdoi:10.1155/2012/694910

Review Article

Chemical Recruitment for Foraging in Ants (Formicidae) and Termites (Isoptera): A Revealing Comparison

Klaus Jaffe, Solange Issa, and Cristina Sainz-Borgo

Departamento de Biología de Organismos, Universidad Simón Bolívar, Caracas 1080, Venezuela

Received 29 April 2011; Revised 30 May 2011; Accepted 31 May 2011

Academic Editor: Jacques H. C. Delabie

Copyright © 2012 Klaus Jaffe et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

All termites secrete trail pheromones from their sternal gland, whereas ants use a variety of glands for this purpose. This and the diversity of chemical compounds that serve as trail pheromones among ants, and the uniformity of chemicals among termite trails, suggest a different evolutionary historical dynamics for the development of chemical mass recruitment in both taxa. Termites in addition show pheromonal parsimony. This suggest a single evolutionary origin of pheromone trails in Isoptera, whereas chemical mass recruitment among Formicidae seems to have evolved many times and in different ways. Despite these very different evolutionary histories, both taxa evolved chemical recruitment systems involving attractants and orientation signals, and at least two divergent decision making system for recruitment. This evolutionary analogy suggests that chemical mass recruitment is constraint by fundamental physical dynamic laws. Artificial intelligence including “mass intelligence” and “ant intelligence”, emulates mass recruitment in interacting virtual agents in search of optimal solutions. This approach, however, has copied only the “Democratic” recruitment dynamics with a single compound pheromone. Ant and termite evolution shows more sophisticated recruitment dynamics which, if understood properly, will improve our understanding of nature and applications of artificial “swarm intelligence”.

1. Introduction

One of the great advantages of society is the use of large numbers of individuals to perform tasks that a lonely individual is unable to perform [2, 3].One of the most studied group task in social insects is recruitment for food retrieval,after an individual discovers a food source that is much larger than what it can handle on its own. Some of the communication signals modulating this recruitment are based on auditory or visual signals, but the most important communication signal used in recruitment, in the great majority of ant and termite species, is chemical. In recruitment to food, these signals are at least of two different kinds as first detailed for ants [4] : one used to orient workers to the food source, that is trail pheromones; another to attract workers to the trail and thus to the food source, that is attractants for food recruitment. Some species use chemicals for only one of these signals and signal the other function by means of tactile or acoustic signals. An illustrative intermediate recruitment system is called “Tandem Running” [5], where the scout physically carries a nestmate to the food source. In tandem calling [6], the recruiting workers lead nestmates to the newly discovered food source by physically guiding them to the source, sometimes using chemical trails to help orientate to the food. Other species lay chemical trails that fulfill both functions, requiring different chemicals for attracting and orienting ants [7, 8]. These intermediate stages in the evolution of chemical mass recruitment, starting from individual foraging, allow us to suggest phylogenies for recruitment systems illuminating the possible evolutionary history of chemical mass recruitment. Such comparisons suggest that the evolution of chemical recruitment seems to have happened several times, at least in ants [9].

Termites seem also to use both type of chemicals, attractants and orientation signals, in their foraging trails [10, 11], although the details of the chemical communication system used by termites are less well known than in ants.

As both, ants and termites, are terrestrial and arboreal, and that both use chemical mass recruitment, we can compare the different chemical recruitment systems known among ants and among termite in order to extract some general rules.

2. Methods

We explored the existing literature collected by Pherobase [1] for publications on trail pheromones for ants and Isoptera and by Bordereau and Pasteels [12] for additional data on Isoptera. Pherobase, among many other things, reports for Isoptera and for Formicidae all publications mentioning chemicals that had been related to trail pheromones by the author of the publication. Pherobase provides, if available, the exact molecular structure of the chemical and the link to the reference where the trail pheromone was published, grouped by taxonomic or by chemical criteria. Thus, for more details of all references indicated in the Tables, the reader should consult Pherobase for ants and Isoptera, and Bordereau and Pasteels for Isoptera.

3. Results

3.1. Ants

Reports of the chemical nature of the communication signal used for recruitment in ants revealed an interesting pattern of chemical compounds. The summary of available data for ants is presented in Table 1. This table shows that, in many cases, the various compounds produced by a single species are very similar as they constitute small variants of a common chemical skeleton, as is the case for Monomorium pharaonis. We suggest that this might be due to the fact that in the biochemical process leading to the synthesis of one or a few active compounds, other chemicals are produced in the process. Indirect evidence for this suggestion comes from other insects where it was shown that synthesizing pure chemicals in pheromone secreting glands is very difficult, if not impossible [13]. In other cases, an adaptive purposeful chemical diversity seems to be present, as chemicals from completely different biochemical pathways are produced as a substrate for the chemical recruitment signal. This is the case for the Atta and Acromyrmex species and Daceton armigerum. In these cases, as shown in Table 1, some compounds have high carbon numbers and low volatility, and others have high volatility, appropriate for the fulfillment of different communication functions such as orientation and attraction.

Table 1: Chemical compounds reported in trail pheromones of ants. All data were extracted from Pherobase [1].

Myrmicinae

Acromyrmex octospinosus

Cross JH 1982. J. Chem. Ecol. 8 : 1119

    me-4me-pyrrole-2-carboxylate

    2me5me-3-ethylpyrazine

    3me5me-2-ethylpyrazine

Acromyrmex subterraneus subterraneus

Do Nascimento RR 1994. J. Chem. Ecol. 20 : 1719

    me-4me-pyrrole-2-carboxylate

Aphaenogaster albisetosus

Hölldobler B 1995 J. Insect Physiol. 41 : 739

    4Sme-7-3Kt

    4Rme-7-3Kt

Aphaenogaster cockerelli

Hölldobler B 1995. J. Insect Physiol. 41 : 739

    1R-phenylethanol

    4Sme-7-3Kt

Aphaenogaster rudis

Attygalle AB 1998b Naturwissenschaften 85 : 38

    anabasine

    anabaseine

    2,3-bipyridyl

    isopentyl-2-phenylethylamine

Atta bisphaerica

De Oliveira JS 1990 An. Soc. Entomol. Brasil 19 : 145

    me-4me-pyrrole-2-carboxylate

    2me5me-3-ethylpyrazine

    2-phenylacetic acid

    bornylene

    8OH

Atta cephalotes

Evershed RP 1983 Insect Biochem. 13 : 469

    me-4me-pyrrole-2-carboxylate

    2me5me-3-ethylpyrazine

    2Ald

Riley RG 1974b J. Insect Physiol. 20 : 651

    me-4me-pyrrole-2-carboxylate

Atta laevigata

De Oliveira JS 1990 An. Soc. Entomol. Brasil 19 : 145

    me-4me-pyrrole-2-carboxylate

    2-phenylacetic acid

    bornylene

    8OH

Atta sexdens

Robinson SW 1978 Bull. Entomol. Res. 68 : 159

    me-4me-pyrrole-2-carboxylate

Atta sexdens rubropilosa

Evershed RP 1983 Insect Biochem. 13 : 469

    me-4me-pyrrole-2-carboxylate

    2me5me-3-ethylpyrazine

    2Ald

Cross JH 1979 J. Chem. Ecol. 5 : 187

    2me5me-3-ethylpyrazine

    methyl phenylacetate

    ethyl phenylacetate

    me-4me-pyrrole-2-carboxylate

Atta sexdens sexdens

Billen J 1992 Ethol. Ecol. Evol. 4 : 197

    2me5me-3-ethylpyrazine

    me-4me-pyrrole-2-carboxylate

Evershed RP 1983 Insect Biochem. 13 : 469

    me-4me-pyrrole-2-carboxylate

    2me5me-3-ethylpyrazine

    2Ald

Atta texana

Tumlinson JH 1972b J. Insect Physiol. 18 : 809

    me-4me-pyrrole-2-carboxylate

Sonnet PE 1972 J. Agric. Food Chem. 20 : 1191

    me-4me-pyrrole-2-carboxylate

Crematogaster castanea

Morgan ED 2004 Chemoecology 14 : 119

    R-dodecan-2-ol

Daceton armigerum

Morgan ED 1992 J. Chem. Ecol. 18 : 2161

    2me5me-pyrazine

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

    delta9-23Hy

    23Hy

    delta9-25Hy

Eutetramorium mocquerysi

Tentschert J 2000 Naturwissenschaften 87 : 377

    2me3me-5-2-methylpropylpyrazine

Manica rubida

Attygalle AB 1986a Physiol. Entomol. 11 : 125

    2me5me-3-ethylpyrazine

Mayriella overbecki

Kohl E 2000 Naturwissenschaften 87 : 320

    me-2-hydroxy-6me-benzoate

Messor bouvieri

Jackson BD 1989a Experientia 45 : 487

    anabasine

    2me5me-3-ethylpyrazine

Messor capensis

Brand JM 1993 J. Chem. Ecol. 19 : 1315

    anabasine

    anabaseine

Messor ebeninus

Coll M 1987 Z. Naturforsch. C 42 : 1027

    anabasine

Metapone madagascarica

Hölldobler B 2002 Chemoecology 12 : 147

    me-pyrrole-2-carboxylate

Metapone madagascarica

Hölldobler B 2002 Chemoecology 12 : 147

    me-pyrrole-2-carboxylate

Monomorium pharaonis Linnaeus

Edwards JP 1978 Ann. Appl. Biol. 89 : 395

    3-butyl-5me-octahydroindolizine

Ritter FJ 1977b Crop Prot. Agents : 195

    monomorine I

Ritter FJ 1977a Tetrahedron Lett. 30 : 2617

    faranal

Ritter FJ 1975b Uni. Dijon : 99

    monomorine I

    monomorine II

    monomorine III

    monomorine IV

    monomorine V

Pheidole pallidula

Ali MF 1988c Physiol. Entomol. 13 : 257

    2me5me-3-ethylpyrazine

Pogonomyrmex barbatus

Liu Y 2002 Fenxi Huaxue 47 : 369

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

    2me5me-pyrazine

Hölldobler B 2001 J. Insect Physiol. 47 : 369

    2me5me-pyrazine

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

Pogonomyrmex maricopa

Hölldobler B 2001 J. Insect Physiol. 47 : 369

    2me5me-pyrazine

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

Pogonomyrmex occidentalis

Hölldobler B 2001 J. Insect Physiol. 47 : 369

    2me5me-pyrazine

    2me3me5me-pyrazine

Pogonomyrmex rugosus

Hölldobler B 2001 J. Insect Physiol. 47 : 369

    2me5me-pyrazine

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

Solenopsis invicta

Van der Meer RK 1983 Fla. Entomol. 66 : 39

    Z,E-alpha-farnesene

    E,E-alpha-farnesene

    Z,E-alpha-homofarnesene

    Z,Z-alpha-homofarnesene

    17Hy

    Z,Z,Z-allofarnesene

Williams HJ 1981b Experientia 37 : 1159

    Z,Z,Z-allofarnesene

Van der Meer RK 1981 Tetrahedron Lett. 22 : 1651

    Z,E-alpha-farnesene

    E,E-alpha-farnesene

    Z,E-alpha-homofarnesene

    Z,Z-alpha-homofarnesene

Tetramorium caespitum

Attygalle AB 1984J. Chem. Ecol. 10 : 1453

    2me5me-pyrazine

    2me5me-3-ethylpyrazine

Attygalle AB 1983b Naturwissenschaften 70 : 364

    2me5me-pyrazine

    2me5me-3-ethylpyrazine

Tetramorium impurum

Morgan ED 1990 J. Chem. Ecol. 16 : 349

    me-2-hydroxy-6me-benzoate

Morgan ED 1987 Naturwissenschaften 74 : 596

    me-2-hydroxy-6me-benzoate

Tetramorium meridionale Emery

Jackson BD 1990c Naturwissenschaften 77 : 294

    2me-pyrazine

    2me5me-pyrazine

    2me3me5me-pyrazine

    2me5me-3-ethylpyrazine

Formicinae

Camponotus atriceps

Haak U 1996 Chemoecology 7 : 85

    6-butyl-tetrahydro-3me5me-pyran-2Kt

    nerolic acid

Camponotus balzani

Kohl E 2003 Chemoecology 13 : 113

    8-hydroxy-3me5me7me-isochromanone

Camponotus castaneus

Kohl E 2003 Chemoecology 13 : 113

    6-butyl-tetrahydro-3me5me-pyran-2Kt

Camponotus floridanus

Haak U 1996 Chemoecology 7 : 85

    6-butyl-tetrahydro-3me5me-pyran-2Kt

    nerolic acid

Camponotus herculeanus

Bestmann HJ 1999 Chem. Eur. J. 5 : 2984

    2Sme4Rme5S-5-hexanolide

Payne TL 1975 Ann. Entomol. Soc. Am. 68 : 385

    me-2-hydroxy-6me-benzoate

    mellein

Hölldobler B 1965 Z. vergl. Physiol. 50 : 551

    me-2-hydroxy-6me-benzoate

    mellein

    10me-12Acid

Camponotus inaequalis

Bestmann HJ 1997 Angew. Chem. 36 : 395

    3,4-dihydro-8-hydroxy-3me5me7me-isocoumarin

Camponotus ligniperda

Bestmann HJ 1999 Chem. Eur. J. 5 : 2984

    2Sme4Rme5S-5-hexanolide

Bestmann HJ 1999 Chem. Eur. J. 5 : 2984

    2Sme4Rme5S-5-hexanolide

Camponotus rufipes

Uebler E 1995 Naturwissenschaften 82 : 523

    mellein

Camponotus sericeiventris

Kohl E 2003 Chemoecology 13 : 113

    8-hydroxy-3me5me7me-isochromanone

Camponotus silvicola

Uebler E 1995 Naturwissenschaften 82 : 523

    8-hydroxy-3me5me7me-isochromanone

Camponotus socius

Kohl E 2001 Chemoecology 11 : 67

    2Sme4Rme5S-5-hexanolide

    2,3-dihydro-3,5-dihydroxy-6me-pyran-4Kt

Bestmann HJ 1999 Chem. Eur. J. 5 : 2984

    2Sme4Rme5S-5-hexanolide

Formica rufa

Bestmann HJ 1992 Angew. Chem. 31 : 795

    R-mellein

Lasius fuliginosus

Kern F 1997 J. Chem. Ecol.23 : 779

    mellein

    2,3-dihydro-3,5-dihydroxy-6me-pyran-4Kt

Akino T 1996 Jap. J. Appl. Entomol. Zool.40 : 233

    caproic acid

    enanthic acid

    caprylic acid

    pelargonic acid

    caprinic acid

    lauric acid

Huwyler S 1975 J. Insect Physiol. 21 : 779

    caproic acid

    enanthic acid

    caprylic acid

    pelargonic acid

    caprinic acid

    lauric acid

Lasius niger

Bestmann HJ 1992 Angew. Chem.31 : 795

    3,4-dihydro-8-hydroxy-3me5me7me-isocoumarin

Linepithema humile

Greenberg L 2000 J. Econ. Entomol. 93 : 119

Cordova YL 1998 Eur. J. Entomol.95 : 501

    sulcatone

    sulcatol

    13-2Kt

    Z9-16Ald

Van Vorhis Key SE 1982 J. Chem. Ecol. 8 : 3

    Z9-16Ald

Cavill GWK 1979 Experientia 35 : 989

    Z9-16Ald

Dolichoderinae

Dolichoderus thoracicus

Attygalle AB 1998a Naturwissenschaften 85 : 275

    Z9-18Ald

    Z9-16Ald

Tapinoma simrothi

Simon T 1991 Insectes Soc. 38 : 17

    iridodial

    iridomyrmecin

Ectatomminae

Ectatomma ruidum

Bestmann HJ 1995 Naturwissenschaften 82 : 334

    geranylgeraniol acetate

    geranylgeraniol

Gnamptogenys striatula

Blatrix R 2002 J. Chem. Ecol. 28 : 2557

    4-methylgeraniol

    bishomogeraniol

    E2,4S6-3me4me7me-octadienyl decanoate

    E2,4S6-3me4me7me-octadienyl dodecanoate

Ponerinae

Leptogenys diminuta

Kern F 1993 Naturwissenschaften 80 : 424

    3R4Sme-heptan-3-ol

Attygalle AB 1991b Naturwissenschaften 78 : 90

    isogeraniol

Attygalle AB 1988c Naturwissenschaften 75 : 315

    3R4Sme-heptan-3-ol

    isogeraniol

Leptogenys peuqueti

Janssen E 1997b Naturwissenschaften 84 : 122

    1-ethyl-4me-heptyl acetate

    1-isopropyl-4me-heptyl acetate

    1-propyl-4me-heptyl acetate

    4me-dodecan-7-ol

    3me9me-dodecan-6-ol

    1-pentyl-4me-heptyl acetate

    4me-tridecan-7-ol

    4me10me-tridecan-7-ol

    4me-tetradecan-7-ol

    3me-hexyl-4me-heptyl acetate

    3me-hexyl-octyl acetate

    heptyloctyl acetate

    4me-hexadecan-7-ol

    3me-hexyl-decyl acetate

Megaponera foetens

Janssen E 1995 J. Chem. Ecol. 21 : 1947

    dimethyluracil

    actinidine

Longhurst C 1979 J. Chem. Ecol. 5 : 703

    1me2me-disulfane

    1me3me-trisulfane

    benzyl methyl sulfane

Longhurst C 1979 J. Chem. Ecol. 5 : 703

    11Hy

    13Hy

Pachycondyla tarsata

Janssen E 1999 Chemoecology 9 : 9

    17-9Kt

Rhytidoponera metallica

Meinwald J 1983Naturwissenschaften 70 : 46

    isogeraniol

    3-hydroxybenzaldehyde

Aenictinae (dorylinae)

Aenictus sp

Oldham NJ 1994, Experientia 50 : 763

    methyl anthranilate

    methyl nicotinate

The chemical survey presented in Table 1 reveals that the pattern of chemical compounds related to trail pheromones in ants correlates with what we know about the decision making behavior used during chemical mass recruitment to food [14]. We know that ants use either one of two decision making systems regulating chemical mass recruitment. The “Democratic” mass recruitment was described in detail for Solenopsis invicta [15] and the “Autocratic” system first described for Atta cephalotes [16]. The main difference is that in the Democratic system, all workers eventually perform all tasks as in Solenopsis; in the Autocratic system, workers specialize either in scouting or in food retrieval [17], as in Atta. The Democratic recruitment system is adapted for fast recruitment towards ephemeral food sources. Here all workers participating in the recruitment process have the same responsibility and add a fixed amount of recruitment pheromone to the trail. The more trail pheromone, the stronger the signal, the more workers are recruited. This leads to an increase in the workforce allowing engaging the maximum worker strength in the shortest possible time, so as to collect a scarce recourse (a recently discovered dead cockroach for example) before a competitor does.

The Autocratic recruitment system is adapted for the simultaneous exploitation of a diversity of durable food sources. Here workers specialize in chemical communication or in food retrieval. Communication specialists then visit different food sources and signal the palatability, quality, or quantity of a food source with varying levels of chemical concentrations. Thus, a very good food source will trigger trail laying with plenty of an attractive chemical, whereas food sources of low quality will be signaled with low amounts of this chemical laid on the trail. This system allows for the fine tuning of sophisticated recruitment activity such as described for several Atta species, where one group of workers recruit nestmates to the tree canopy where they cut large leaves at their base, so that they fall whole to the ground. There, another group of workers is recruited to each of the leaves that accumulate on the ground, where the workers cut the leave in smaller pieces and transport these pieces to intermediate sites, from where another group of workers transport the leaf fragments to the nest [18].

In both cases, the trail needs to be marked with a chemical that will orient workers towards the food source. If the food source is ephemeral in its existence, an efficient chemical mark does not need to last long. As soon as the food has been collected, the chemical evaporates and the trail disappears. For the simultaneous exploitation of several food sources, however, several longer lasting chemical signals could be very useful, as the source could be revisited fast after spots of inactivity due to rain, heat, cold, or other daily rhythmic patterns. Yet a long lasting chemical signal is not appropriate if it has to work also as an attractant, as any changes in the required workforce will take a long time to achieve if the long lasting chemical need, to evaporate first. Therefore in this later case, highly volatile chemicals, together with some of low volatility, are required to modulate recruitment. Species using chemicals to only attract or orient ants need only one—or a few—chemical compounds to perform this function, whereas species using chemical trails for both, attraction and orientation of nestmates, have to produce a range of chemicals for these two purposes.

As Table 1 shows, most ant species seem to use a few compounds as trail pheromone. Only 14 out of 57 species (25%) seem to use more than 3 chemicals, and only 10% of the species listed use six or more compounds. The use of a few compounds corresponds well to Tandem Calling or even to a Democratic recruitment system. In contrast, species such as the leaf cutting and fungus growing ants Atta, Trachymyrmex, and Acromyrmex secrete over six different chemicals on their trails. Other species using the Democratic system, such as Solenopsis, seem to produce much simpler trail pheromones from the standpoint of chemical diversity of compounds. The trail pheromone composition of Solenopsis invicta recalls the case of Monomorium pharaonis discussed above. Although over 5 different chemicals can be recognized in Table 1, all these chemicals have the same chemical skeleton. Thus, the Autocratic chemical recruitment system could be associated to a more advanced chemical signaling. The case of the hunting and recruiting foragers of Daceton armigerum [19] that use a multitude of recruitment strategies is interesting. Table 1 shows that its trail pheromone has many chemical compounds, hinting to a sophisticated diverse chemical communication system.

Many ant species in the subfamily Myrmicinae with large colonies and a sophisticated social structure, use carboxylates and pyrazines to lay their pheromone trail. These are semivolatile compounds. The Myrmicinae, Atta, and Acromyrmex, for example, need to constantly recruit many workers to supply big colonies with a great quantity of leaves which they use as a substrate to grow their fungus. In contrast, ants with less developed societies living in smaller colonies, such as species of the subfamily Ponerinae, use alcohols and acetate, which are more volatile and thus might serve as chemical attractants to trigger foraging to collect ephemeral food sources. Ponerinae individuals feed opportunistically on dispersed food items. This requires quick recruitment of workers, and, as a consequence, the compounds of the pheromone trail are more volatile and less permanent in time, compared to the carboxylates of the leaf cutter ants. In some species of Ponerinae, chemical trails also regulate nest moving [20].

The Formicinae ants are mostly predators but differ from Ponerinae by their greater social complexity, larger colonies, and more diverse worker castes or polymorphism. The trail pheromones of Formicinae species use a mix of compounds that are more complex than that of Ponerinae, probably due to a more elaborate recruitment system. Table 1 reflects this showing among Formicinae, compounds with elevated molecular weights, such as mullein, in addition to compound of low molecular weight and probably low volatility. Formicinae trail pheromone chemistry seems to be closer to the Myrmicinae than the Ponerinae. This suggests trails with both short-term attractant and long-term orientation function. In the case of Dolichoderinae species, the information is scarcer. In the Argentine ant, Linepithema humile, a tramp species with supercolonies of hundreds of thousands of workers, the trail pheromone has short-chain volatile aldehydes, suggesting a foraging strategy with fast short term bouts of recruitment. The continuous reinforcement of a trail made with short lasting volatiles can last long if it is reinforced by hundreds of workers.

3.2. Termites

Termite species also show diverse ecological life types. We know species that live and feed in the same piece of wood, and species that have their nest separated from their food source [21]. But even the “one-piece” life type species possess trail pheromones which they use to recruit workers for defense or nest moving. Termites of “one-piece” life type do not require orientation systems a priori. Secretions of their sternal gland are considered to function in the recruitment of nestmates to source disturbance within the nest. These termites might also use trail following pheromones to colonize new food sources to where they move their nest [22, 23]. Most termites forage on relatively durable food sources containing cellulose. In addition, most termite species forage on several food sources simultaneously, suggesting a recruitment system closer to the above described Autocratic chemical recruitment system, which seem to be the case in the only termite species where this has been explored so far [24]. Table 2 presents what we know about the chemicals used in trail pheromones by termites. The available data shows that pheromone trails among each termite species are constructed with one or a few compounds among a total of 8 chemicals. For the families where chemical trail pheromones have been reported, the Rhinotermitidae, Termitidae, and Kalotermitidae seem to use mainly neocembrene and a dodecatrienol; Nasutitermes corniger uses in addition to these two compounds trinervitatriene; whereas Mastotermitidae and Termopsidae use a trimethylundecadienol for trail following. That is, all trail pheromones in Isoptera are synthesized from a much conserved metabolic route eventually leading to a compound with the same carbon skeleton as that of a dodecatrienol, where two subfamilies have diverged somewhat from the rest in that they synthesize trimethylundecadienol instead of dodecatrienol as the rest of termite species does.

Table 2: Chemical compounds reported from trail pheromones of termites. All data were extracted from Pherobase [1], and from Bordereau and Pasteels [12].

Mastotermitidae

Mastotermes darwiniensis

Sillam-Dussès, D. et al. 2007. J Chem. Ecol 33 : 1960–1977

    (E)-2,6,10-trimethyl-5,9-undecadien-1-ol

Termopsidae

Porotermitinae

Porotermes adamsoni

Sillam-Dussès, D. et al. 2007. J Chem. Ecol 33 : 1960–1977

    (E)-2,6,10-trimethyl-5,9-undecadien-1-ol

Stolotermitinae

Stolotermes victoriensis

Sillam-Dussès, D. et al. 2007. J Chem. Ecol 33 : 1960–1977

    (E)-2,6,10-trimethyl-5,9-undecadien-1-ol

Termopsinae

Zootermopsis angusticollis

Greenberg SL 1986 Int. J. Insect Morphol. Embryol. 15 : 283

    Heneicosano

    Tricosane

Bordereau C. et al. 2010 Biol J Linn Soc 100 : 519–530

    4,6-dimethyldodecanal

Zootermopsis nevadensis

Karlson P. et al. 1968 J. Insect Physiol. 14 : 1763

    n-Hexanoic acid

    Caproic acid

Bordereau, C. et al. 2010 Biol J Linn Soc 100 : 519–530

    4,6-Dimethyldodecanal

Kalotermitidae

Cryptotermes brevis

Sillam-Dussès D. et al. 2009 Chemoecology19 : 103–108

    (Z)-dodec-3-en-1-ol

Cryptotermes darlingtonae

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Cryptotermes pallidus

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Incisitermes tabogae

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Kalotermes flavicollis

Klochkov and Zhuzhikov 1990. Advances in life science. Birkhäuser, Basel, pp 41–43

    Nonanol

    Decanol

    Undecanol

    dodecanol

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Neotermes holmgreni

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Postelectrotermes howa

Sillam-Dussès et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Procryptotermes falcifer

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Procryptotermes leewardensis

Sillam-Dussès D. et al. 2009 Chemoecology 19 : 103–108

    (Z)-dodec-3-en-1-ol

Rhinotermitidae

Prorhinotermitinae

Prorhinotermes canalifrons

Sillam-Dussès D. et al. 2005 Chemoecology 15 : 1–6

    Neocembrene A

Prorhinotermes simplex

Sillam-Dussès D. et al. 2005 Chemoecology 15 : 1–6

    Neocembrene

Sillam-Dussès D. et al. 2009 J. Insect Physiol 55  : 751-757

    Neocembrene A

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Coptotermitinae

Coptotermes formosanus

Tokoro M. et al. 1994 J. Chem. Ecol. 20 : 199

    (Z,E,E)-dodeca-3,6,8-trien-1-ol

Coptotermes gestroi

Arab A. et al. 2004 Sociobiology 43 : 377

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Sillam-Dussès D. et al. 2006 Proceedings XV IUSSI. Washington 100-101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Heterotermitinae

Heterotermes tenuis

Arab A. et al. 2004 Sociobiology 43 : 377

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Sillam-Dussès D. et al. 2006 Proceedings XV IUSSI. Washington 100-101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes flavipes

Howard R. et al. 1976 J. Chem. Ecol. 2 : 147

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Matsumura F. et al. 1968 Nature 219 :  963

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes hesperus

Zhong CM 1979 Sci. Silvae Sin. 15 : 15

    Z3-4-phenyl-4OH

Reticulitermes lucifugus grassei

Wobst B. et al. 1999 J. Chem. Ecol. 25 : 1305

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes santonensis

Wobst B. et al. 1999 J. Chem. Ecol. 25 : 1305

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Laduguie N. et al. 1994 J. Insect Physiol. 40 : 781

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes speratus

Tokoro M. et al. 1990 J. Chem. Ecol. 16 : 2549

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Yamaoka R. et al. 1987 J. Chromatogr. 399 : 259

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes tibialis

Bernklau EJ 2005 J. Econ. Entomol. 98 : 476

    CO2

Zhong CM 1979 Sci. Silvae Sin. 15 : 15

    Z3-4-phenyl-4OH

Howard R. et al. 1976 J. Chem. Ecol. 2 : 147

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Reticulitermes virginicus

Howard R. et al. 1976 J. Chem. Ecol. 2 : 147

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Tai A. et al. 1969 J. Org. Chem. 34 : 2180

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Matsumura F. et al. 1968 Nature 219 : 963

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Rhinotermitinae

Rhinotermes marginalis

Sillam-Dussès D. et al. 2006 Proc. XV Congress IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Schedorhinotermes lamanianus

Sillam-Dussès D. et al. 2006 Proc. XV Congress IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Termitidae

Macrotermitinae

Ancistrotermes pakistanicus

Robert A. et al. 2004 Naturwissenschaften 91 : 34–39

    (Z,Z)-dodeca-3,6-dien-1-ol

Macrotermes annandalei

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-l-ol

Peppuy A. et al. 2001 J. Insect Physiol. 47 : 445

    (Z)-dodec-3-en-l-ol

Macrotermes barneyi

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-l-ol

Macrotermes bellicosus

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-l-ol

Macrotermes subhyalinus

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-1-ol

Odontotermes formosanus

Deng XJ. et al. 2002 Acta Entomol. Sin. 45 : 739

    (Z,Z)-dodeca-3-6-dien-1-ol

    Du TY 1982 Acta Entomol. Sin. 25 : 172

    (Z,Z)-dodeca-3-6-dien-1-ol

Odontotermes hainanensis

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-1-ol

Odontotermes maesodensis

Peppuy A. et al. 2001 Insectes Soc. 48 : 245

    (Z)-dodec-3-en-1-ol

Pseudacanthotermes militaris

Bordereau C. et al. 1993 Actes Coll. Insectes Soc. 17 : 2177

    (Z,Z,E)-dodeca-3,6,8-trienol-1-ol

Pseudacanthotermes spiniger

Bordereau C. et al. 1991 J. Chem. Ecol. 17 : 2177

    (Z,Z,E)-dodeca-3,6,8-trienol-1-ol

Termitinae

Cubitermes sp.

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Drepanotermes perniger

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Termes hispaniolae

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Amitermes evuncifer

Kotoklo E. et al. 2010 Sociobiology 55 : 1-10

    Dodecatrienol

    Neocembrene A

Syntermitinae

Cornitermes bequaerti

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Cornitermes cumulans

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Cornitermes snyderi

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Syntermes grandis

Sillam-Dussès D. et al. 2006 Proc. IUSSI, Washington, DC, 100–101

    (Z,Z,E)-dodeca-3,6,8-trien-1-ol

Nasutitermitinae

Constrictotermes cyphergaster

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes corniger

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

    Trinervitatriene

Nasutitermes diabolus

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes ephratae

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes exitiosus

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Birch AJ 1972 J. Chem. Soc. 1 : 2653

    Neocembrene-A

Nasutitermes graveolus

Moore P 1966 Nature 211 : 746–747

    Neocembrene-A

Birch A. et al. 1972 J Chem Soc Perkin Trans 1 : 2653–2658

    Neocembrene-A

Nasutitermes guayanae

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes kemneri

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes lujae

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Nasutitermes walkeri

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Neocembrene-A

Nasutitermes voeltzkowi

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Trinervitermes bettonianus

McDowell PG and Oloo G. 1984 J. Chem. Ecol. 10 : 835

    Neocembrene-A

Trinervitermes geminatus

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

Trinervitermes trinervoides

Sillam-Dussès D. et al. 2010 Biol. J. Linnean Soc. 99 : 20

    Dodecatrienol

    Neocembrene-A

In the case of termites, volatile chemicals for modulating the recruitment of workers are most likely to be used outside the nest or outside the covered galleries. This seems natural if we take into account that most termites forage in galleries which orient workers to their food sources. Very volatile chemicals are of little use in closed environments where they cannot disperse. Long-lasting, low-volatility chemicals may be useful for trail orientation outside the nest and might form the substrate around which galleries are built [25]. Thus, other signals seem to be more appropriate here in modulating communication. Many termite species add feces, saliva, and other secretions to the trail. This explains foraging trails that are reused after several years. A different situation may occur among termites foraging on grasses or leaves in open habitats and foraging at the end of their galleries where they can display very sophisticated foraging and recruitment strategies [26]. When recruitment behavior was explored in an open setting in a Nasutitermitinae [24], the decision making systems used to modulate the recruitment dynamics conformed to the Autocratic kind described for Atta.

4. Discussion

This paper is based only on published reports, and many more compounds used as trail pheromones are surely to be discovered in the future. For example, it is very likely that Atta texana uses a larger pool of compounds as trail pheromones as that reported in Table 1, as it is unlikely to differ very much from other Atta species in this regard. Thus, results in the Tables are biased towards species that have drawn more attention from researchers. Another cautionary remark regards the assessment of volatility based on chemical structure alone. In general, compounds of the same kind of lower molecular weight are more volatile than the ones of higher molecular weight or longer carbon chains. Biologically relevant volatility, however, depends not only on the compound but also on the substrate on which the chemical is secreted, on its concentrations on the substrate, and on the humidity and temperature of the surrounding air. Thus, simple direct correlations between molecular weight, assumed volatility, and behavioral function of a compound should be avoided.

The work behind the literature used for this study, evidently, was not performed with our objectives in mind, but it is unlikely that methodological limitations explain the lack of more chemical compound associated with trail pheromones among termites than among ants. Despite many possible limitations of this study, the large extend of the research effort explored and the large number of species covered guarantee a minimum of robustness that makes drawing conclusion from these data reasonable.

Despite these and other limitations of this paper, we might suggest two basic trends: (1) evolutionary history of the evolution of ant and termite trails is very different, and (2) the dynamics of interacting individuals achieving a recruitment process mediated by chemicals follow basic rules.

4.1. Different Evolutionary Histories between Ants and Termites

The diversity of chemical structures among ant trail pheromones and the uniformity of chemical compounds among termite trails suggest a different evolutionary history for the development of chemical mass recruitment in both taxa. In termites, often trail pheromone compounds are synthesized also by other exocrine glands and are used as sex pheromones. This pheromonal parsimony seems to be characteristic of termites [12] and is not common among ants.

Chemical mass recruitment among ants seems to have evolved at least 8 times [9], whereas chemical mass recruitment among termites seems to be a more conservative phenomenon where all species seem to share a common ancestor that had already developed chemical recruitment. This explains also the large difference between ants and termites in the glands responsible for the secretion of the trail pheromones. Many different glands are used by different species among ants [27], whereas only the sternal gland is used by termites [12]. Another factor explaining this difference is the ecological diversity of ant species, each exploring different food source. Termites in contrast exploit more uniform ecological niches in their search for cellulose.

4.2. Basic Rules Govern the Recruitment Dynamics

The main conclusion from this study is that despite the fact that the evolutionary history of the chemical mass recruitment of ants and termites is different, a similar recruitment dynamics has evolved in both groups. This evolutionary analogy suggests that chemical mass recruitment is constraint by basic physical-dynamic laws. This would explain the convergence to chemical mass recruitment in the two evolutionary processes studied. A third convergence towards similar solution for the modulation of mass recruitment dynamics is nowadays repeated in the development of artificial intelligence, where the “mass intelligence” of ants copied in the interaction of simple virtual computer agents is in search of optimal solutions. Artificial intelligence, however, has copied only the simple recruitment dynamics named here as the Democratic system with a single compound pheromone. More sophisticated modeling could bear fruits to artificial intelligence that might echo the fruits chemical mass recruitment that has brought to social insect species evolving them.

References

A. M. El-Sayed, “The pherobase: database of insect pheromones and semiochemicals,” 2008, http://www.pherobase.net.

K. Jaffe, “An economic analysis of altruism: who benefits from altruistic acts?” JASSS, vol. 5, no. 3, 2002.

K. Jaffe, “Quantifying social synergy in insect and human societies,” Behavioral Ecology and Sociobiology, vol. 64, no. 11, pp. 1721–1724, 2010.

K. Jaffe, “Theoretical analysis of the communication system for chemical mass recruitment in ants,” Journal of Theoretical Biology, vol. 84, no. 4, pp. 589–609, 1980.

E. O. Wilson, “Communication by tandem running in the ant genus Cardiocondyla,” Psyche, vol. 66, no. 3, pp. 29–34, 1959.

M. Möeglich, U. Maschwitz, and B. Höelldobler, “Tandem calling: a new kind of signal in ant communication,” Science, vol. 186, no. 4168, pp. 1046–1047, 1974.

K. Jaffe, C. Ramos, C. Lagalla, and L. Parra, “Orientation cues used by ants,” Insectes Sociaux, vol. 37, no. 2, pp. 101–115, 1990.

E. D. Morgan, “Trail pheromones of ants,” Physiological Entomology, vol. 34, no. 1, pp. 1–17, 2009.

K. Jaffe, “Negentropy and the evolution of chemical recruitment in ants,” Journal of Theoretical Biology, vol. 106, no. 4, pp. 587–604, 1984.

G. W. Oloo and R. H. Leuthold, “The influence of food on trail-laying and recruitment behaviour in Trinervitermes bettonianus (Termitidae : Nasutitermitinae),” Entomologia Experimentalis et Applicata, vol. 26, no. 3, pp. 267–278, 1979.

J. Affolter and R. H. Leuthold, “Quantitative and qualitative aspects of trail pheromones in Macrotermes subhyalinus (Isoptera, Termitidae),” Insectes Sociaux, vol. 47, no. 3, pp. 256–262, 2000.

C. Bordereau and J. M. Pasteels, “Pheromones and chemical ecology of dispersal and foraging in termites,” in Biology of Termites: A Modern Synthesis, D. E. Bignell, Y. Roisin, and N. Lo, Eds., Springer, New York, NY, USA, 2011.

B. Mirás, A. Cabrera, and K. Jaffe, “Mate selection in the moth Neoleucinodes elegantalis: evidence for a supernormal chemical stimulus in sexual attraction,” Animal Behaviour, vol. 73, no. 4, pp. 727–734, 2007.

K. Jaffe, Villegas G., Colmenares O., et al., “Two different decision-making systems in recruitment to food in ant societies,” Behaviour, vol. 92, pp. 9–21, 1985.

E. O. Wilson, “Chemical communication among workers of the fire ant (Solenopsis saevissima),” Animal Behaviour, vol. 10, no. 1-2, pp. 134–164, 1962.

K. Jaffe and P. E. Howse, “The mass recruitment system of the leaf- cutting ant Atta cephalotes,” Animal Behaviour, vol. 27, no. 3, pp. 930–939, 1979.

K. Jaffe and J. L. Deneubourg, “On foraging, recruitment systems and optimum number of scouts in ants,” Insectes Sociaux, vol. 39, no. 2, pp. 201–213, 1992.

H. G. Fowler and S. W. Robinson, “Foraging by Atta sexdens: seasonal patterns, caste and efficiency,” Ecological Entomology, vol. 4, pp. 239–247, 1979.

Y. Mady and K. Jaffe, “On foraging behavior of the polymorphic tree dwelling ant Daceton armigerum,” Entomotropica, vol. 21, pp. 117–123, 2006.

B. Gobin, C. Peeters, J. Billen, and E. D. Morgan, “Interspecific trail following and commensalism between the ponerine ant Gnamptogenys menadensis and the formicine ant Polyrhachis rufipes,” Journal of Insect Behavior, vol. 11, no. 3, pp. 361–369, 1998.

P. Eggleton and I. Tayasu, “Feeding groups, lifetypes and the global ecology of termites,” Ecological Research, vol. 16, no. 5, pp. 941–960, 2001.

A. M. Stuart, “Social behavior and communication,” in Biology of Termites, K. Krishna and F. M. Weesner, Eds., vol. 1, pp. 193–232, Academic Press, New York, NY, USA, 1969.

J. F. A. Traniello and R. H. Leuthold, “Behavior and ecology of foraging in termites,” in Termites: Evolution, Sociality, Symbioses, Ecology, T. Abe, D. E. Bignell, and M. Higashi, Eds., pp. 141–168, Kluwer Academic Publisher, Dordrecht, The Netherlands, 2000.

C. Andara, S. Issa, and K. Jaffe, “Decision-making systems in recruitment to food for two nasutitermitinae,” Sociobiology, vol. 44, no. 1, pp. 139–151, 2004.

E. Bonabeau, G. Theraulaz, J. L. Deneubourg, N. R. Franks, O. Rafelsberger, J. L. Joly, and S. Blanco, “A model for the emergence of pillars, walls and royal chambers in termite nests,” Philosophical Transactions of the Royal Society B, vol. 1375, pp. 1561–1576, 1998.

D. Alfonso, Ecología y comportamiento de Syntermes (Isoptera,Termitidae Syntermitinae) en la Gran Sabana, Estado Bolívar, MSc Thesis in Biology, Universidad Simón Bolívar, Caracas, Venezuela, 2011.

J. Billen and E. D. Morgan, “Pheromone communication in social insects: sources and secretions,” in Pheromone Communication in Social insects. Ants, Wasps, Bees, and Termites, R. K. van der Meer, et al., Ed., pp. 3–33, Westview Press, New York, NY, USA, 1998.