Trail pheromones: an integrative view of their role in social insect colony organization.

Trail pheromones do more than simply guide social insect workers from point A to point B. Recent research has revealed additional ways in which they help to regulate colony foraging, often via positive and negative feedback processes that influence the exploitation of the different resources that a colony has knowledge of. Trail pheromones are often complementary or synergistic with other information sources, such as individual memory. Pheromone trails can be composed of two or more pheromones with different functions, and information may be embedded in the trail network geometry. These findings indicate remarkable sophistication in how trail pheromones are used to regulate colony-level behavior, and how trail pheromones are used and deployed at the individual level.

[1]  J. Carthy The Orientation of Two Allied Species of British Ant , 1951 .

[2]  E. Wilson Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith) 1. The Organization of Mass-Foraging , 1962 .

[3]  K. Frisch The dance language and orientation of bees , 1967 .

[4]  M. -. Cammaerts-Tricot Recrutement D'Ouvrieres, Chez Myrmica Rubra, Par Les Pheromones De L'Appareil a Venin , 1974 .

[5]  B. Hölldobler Tournaments and slavery in a desert ant. , 1976, Science.

[6]  M. Cammaerts,et al.  Food recruitment strategies of the ants Myrmica sabuleti and Myrmica ruginodis , 1980, Behavioural Processes.

[7]  B. Hölldobler Trail Communication in the Dacetine Ant Orectognathus Versicolor (Hymenoptera: Formicidae) , 1981 .

[8]  R. Jeanne Chemical communication during swarm emigration in the social wasp Polybia sericea (Olivier) , 1981, Animal Behaviour.

[9]  R. Evershed,et al.  Comparative study of the dufour gland secretions of workers of four species of Myrmica ants , 1981 .

[10]  P. Howse,et al.  Orientation in leaf-cutting ants (Formicidae: Attini) , 1987, Animal Behaviour.

[11]  M. Breed,et al.  Effects of experience on use of orientation cues in the giant tropical ant , 1989, Animal Behaviour.

[12]  Jean-Louis Deneubourg,et al.  Collective flexibility during mass recruitment in the ant Myrmica sabuleti (Hymenoptera: Formicidae) , 1991 .

[13]  J. Deneubourg,et al.  Trails and U-turns in the Selection of a Path by the Ant Lasius niger , 1992 .

[14]  Francisco J. Acosta,et al.  Branching angles of ant trunk trails as an optimization cue , 1993 .

[15]  Trail communication in the ant Megaponera foetens (Fabr.) (Formicidae, Ponerinae) , 1994 .

[16]  Jean-Louis Deneubourg,et al.  The dynamics of collective exploration and trail‐formation in Monomorium pharaonis: experiments and model , 1994 .

[17]  James F. A. Traniello,et al.  Trail and Territorial Communication in Social Insects , 1995 .

[18]  E. Morgan,et al.  Recruitment pheromones in the ants Aphaenogaster albisetosus and A. cockerelli (Hymenoptera: Formicidae) , 1995 .

[19]  The role of trunk trails in the scouting activity of the leaf-cutting ant Atta cephalotes , 1998 .

[20]  S. Levin Ecosystems and the Biosphere as Complex Adaptive Systems , 1998, Ecosystems.

[21]  Guy Theraulaz,et al.  The origin of nest complexity in social insects , 1998 .

[22]  Guy Theraulaz,et al.  The origin of nest complexity in social insects , 1998, Complex..

[23]  B. Hōlldobler Multimodal signals in ant communication A Neuroethology, sensory, neural, and behavioral physiology , 1999 .

[24]  Deborah M. Gordon,et al.  Encounter rate and task allocation in harvester ants , 1999, Behavioral Ecology and Sociobiology.

[25]  Nigel R. Franks,et al.  Ants estimate area using Buffon's needle , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  J. J. Howard Costs of trail construction and maintenance in the leaf-cutting ant Atta columbica , 2001, Behavioral Ecology and Sociobiology.

[27]  S. Lloyd,et al.  Measures of complexity: a nonexhaustive list , 2001 .

[28]  Thomas S. Collett,et al.  Memory use in insect visual navigation , 2002, Nature Reviews Neuroscience.

[29]  M. Breed,et al.  Time-place learning and the ecology of recruitment in a stingless bee, Trigona amalthea (Hymenoptera, Apidae) , 2002 .

[30]  C. Detrain,et al.  Collective exploration and area marking in the ant Lasius niger , 2002, Insectes Sociaux.

[31]  D. Cassill,et al.  Rules of supply and demand regulate recruitment to food in an ant society , 2003, Behavioral Ecology and Sociobiology.

[32]  D. Sumpter,et al.  From nonlinearity to optimality: pheromone trail foraging by ants , 2003, Animal Behaviour.

[33]  U. Maschwitz,et al.  Recruitment gland of Leptogenys chinensis , 1977, Naturwissenschaften.

[34]  W. Cochran,et al.  Migrating Songbirds Recalibrate Their Magnetic Compass Daily from Twilight Cues , 2004, Science.

[35]  M. Lindauer,et al.  Die gegenseitige Verständigung bei den stachellosen Bienen , 1958, Zeitschrift für vergleichende Physiologie.

[36]  W. Hangartner Spezifität und Inaktivierung des Spurpheromons von Lasius fuliginosus Latr. und Orientierung der Arbeiterinnen im Duftfeld , 1967, Zeitschrift für vergleichende Physiologie.

[37]  Claire Detrain,et al.  Out of sight but not out of mind: modulation of recruitment according to home range marking in ants , 2004, Animal Behaviour.

[38]  J. Deneubourg,et al.  Self-organized shortcuts in the Argentine ant , 1989, Naturwissenschaften.

[39]  Edward O. Wilson,et al.  The multiple recruitment systems of the african weaver ant Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae) , 1978, Behavioral Ecology and Sociobiology.

[40]  F. Ratnieks,et al.  Trail geometry gives polarity to ant foraging networks , 2004, Nature.

[41]  B. Hölldobler Foraging and spatiotemporal territories in the honey ant Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae) , 1981, Behavioral Ecology and Sociobiology.

[42]  J. Traniello Recruitment and orientation components in a termite trail pheromone , 1982, Naturwissenschaften.

[43]  H. Markl,et al.  Recruitment and food-retrieving behavior in Novomessor (Formicidae, Hymenoptera) , 1978, Behavioral Ecology and Sociobiology.

[44]  B. Hölldobler Recruitment behavior, home range orientation and territoriality in harvester ants, Pogonomyrmex , 1976, Behavioral Ecology and Sociobiology.

[45]  S. Turillazzi,et al.  Nest-area marking with faeces: a chemical signature that allows colony-level recognition in seed harvesting ants (Hymenoptera, Formicidae) , 2005, Insectes Sociaux.

[46]  B. Hölldobler,et al.  Recruitment and food-retrieving behavior in Novomessor (Formicidae, Hymenoptera) , 1978, Behavioral Ecology and Sociobiology.

[47]  James F. A. Traniello,et al.  Social organization and foraging success in Lasius neoniger (Hymenoptera: Formicidae): behavioral and ecological aspects of recruitment communication , 1983, Oecologia.

[48]  A. J. Moore,et al.  Graded recruitment in a ponerine ant , 1987, Behavioral Ecology and Sociobiology.

[49]  B. Hölldobler Recruitment behavior in Camponotus socius (Hym. Formicidae) , 1971, Zeitschrift für vergleichende Physiologie.

[50]  F. Kern,et al.  Communication in the migratory termite-hunting ant Pachycondyla (= Termitopone) marginata (Formicidae, Ponerinae) , 2004, Journal of Comparative Physiology A.

[51]  J. Nieh,et al.  Polarized short odor-trail recruitment communication by a stingless bee, Trigona spinipes , 2004, Behavioral Ecology and Sociobiology.

[52]  J. Deneubourg,et al.  Memory and chemical communication in the orientation of two mass-recruiting ant species , 1993, Insectes Sociaux.

[53]  J. Deneubourg,et al.  The self-organizing exploratory pattern of the argentine ant , 1990, Journal of Insect Behavior.

[54]  J. Verhaeghe,et al.  Food recruitment inTetramorium impurum (Hymenoptera: Formicidae) , 1982, Insectes Sociaux.

[55]  W. Hangartner Orientierung vonLasius fuliginosus Latr. an einer Gabelung der Geruchsspur , 1969, Insectes Sociaux.

[56]  R. Rosengren,et al.  Ortstreue in foraging ants of theFormica rufa group — Hierarchy of orienting cues and long-term memory , 1986, Insectes Sociaux.

[57]  J. Traniello Colony specificity in the trail pheromone of an ant , 1980, Naturwissenschaften.

[58]  J. Deneubourg,et al.  Modulation of trail laying in the antLasius niger (Hymenoptera: Formicidae) and its role in the collective selection of a food source , 1993, Journal of Insect Behavior.

[59]  J. Traniello,et al.  Behavioral bioassays of termite trail pheromones , 1985, Journal of Chemical Ecology.

[60]  J. Deneubourg,et al.  Trail laying behaviour during food recruitment in the antLasius niger (L.) , 1992, Insectes Sociaux.

[61]  B. Hölldobler,et al.  The foraging system ofPheidole militicida (Hymenoptera: Formicidae) , 1980, Insectes Sociaux.

[62]  Christina D. Runcie Behavioral evidence for multicomponent trail pheromone in the termite,Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae) , 1987, Journal of Chemical Ecology.

[63]  V. Fourcassié,et al.  How do red wood ants orient when foraging in a three dimensional system? I. Laboratory experiments , 1988, Insectes Sociaux.

[64]  C. Detrain,et al.  How does food distance influence foraging in the ant Lasius niger: the importance of home-range marking , 2005, Insectes Sociaux.

[65]  J. Deneubourg,et al.  Collective decision making through food recruitment , 1990, Insectes Sociaux.

[66]  Mike Holcombe,et al.  Insect communication: ‘No entry’ signal in ant foraging , 2005, Nature.

[67]  F. Ratnieks,et al.  Longevity and detection of persistent foraging trails in Pharaoh's ants, Monomorium pharaonis (L.) , 2006, Animal Behaviour.

[68]  Guy Theraulaz,et al.  Path efficiency of ant foraging trails in an artificial network. , 2006, Journal of theoretical biology.

[69]  A. Attygalle,et al.  Complex chemical communication in the crazy ant Paratrechina longicornis Latreille (Hymenoptera: Formicidae) , 2007, Chemoecology.

[70]  J. Deneubourg,et al.  Starvation drives a threshold triggering communication , 2006, Journal of Experimental Biology.

[71]  F. Ratnieks,et al.  Communication in ants , 2006, Current Biology.

[72]  Anna Dornhaus,et al.  Reconnaissance and latent learning in ants , 2007, Proceedings of the Royal Society B: Biological Sciences.

[73]  Marco Dorigo,et al.  Ant colony optimization , 2006, IEEE Computational Intelligence Magazine.

[74]  Lars Chittka,et al.  Social Learning in Insects — From Miniature Brains to Consensus Building , 2007, Current Biology.

[75]  Francis L. W. Ratnieks,et al.  Biomimicry: Further Insights from Ant Colonies? , 2008, BIOWIRE.

[76]  Deborah M Gordon,et al.  How Patrollers Set Foraging Direction in Harvester Ants , 2007, The American Naturalist.

[77]  Smelling the past David S Barnes The Great Stink of Paris and the Nineteenth-Century Struggle Against Filth and G , 2007, The Lancet.

[78]  Elva J H Robinson,et al.  An agent-based model to investigate the roles of attractive and repellent pheromones in ant decision making during foraging. , 2008, Journal of theoretical biology.

[79]  Owen L. Petchey,et al.  Combined use of pheromone trails and visual landmarks by the common garden ant Lasius niger , 2008, Behavioral Ecology and Sociobiology.

[80]  Guy Theraulaz,et al.  Are ants sensitive to the geometry of tunnel bifurcation? , 2008, Animal Cognition.

[81]  M. Hrncir,et al.  11 Mobilizing the Foraging Force Mechanical Signals in Stingless Bee Recruitment , 2009 .

[82]  Stefan Jarau,et al.  Chemical Communication during Food Exploitation in Stingless Bees , 2009 .

[83]  A. Dussutour,et al.  Noise improves collective decision-making by ants in dynamic environments , 2009, Proceedings of the Royal Society B: Biological Sciences.

[84]  D. Sumpter,et al.  The role of multiple pheromones in food recruitment by ants , 2009, Journal of Experimental Biology.

[85]  E. Morgan Trail pheromones of ants. , 2009 .

[86]  M. Hrncir,et al.  Food Exploitation By Social Insects : Ecological, Behavioral, and Theoretical Approaches , 2009 .

[87]  P. Graham,et al.  Ants use the panoramic skyline as a visual cue during navigation , 2009, Current Biology.

[88]  Chemical Communication during Food Exploitation in Stingless Bees , 2009 .

[89]  C. Detrain,et al.  Hydrocarbons in the Ant Lasius niger: From the Cuticle to the Nest and Home Range Marking , 2009, Journal of Chemical Ecology.

[90]  Jean-Louis Deneubourg,et al.  Social Cues and Adaptive Foraging Strategies in Ants , 2009 .

[91]  S. Jarau,et al.  Stingless bees (Scaptotrigona pectoralis) learn foreign trail pheromones and use them to find food , 2011, Journal of Comparative Physiology A.

[92]  J. Pasteels,et al.  Pheromones and Chemical Ecology of Dispersal and Foraging in Termites , 2010 .

[93]  F. Ratnieks,et al.  Decision making in ant foragers (Lasius niger) facing conflicting private and social information , 2011, Behavioral Ecology and Sociobiology.

[94]  N. Franks,et al.  Improving Decision Speed, Accuracy and Group Cohesion through Early Information Gathering in House-Hunting Ants , 2010, PloS one.

[95]  H. Roche,et al.  Why Copy Others? Insights from the Social Learning Strategies Tournament , 2010 .

[96]  A. Farji-Brener,et al.  Information transfer in head-on encounters between leaf-cutting ant workers: food, trail condition or orientation cues? , 2010, Animal Behaviour.

[97]  J. Deneubourg,et al.  Recruitment in starved nests: the role of direct and indirect interactions between scouts and nestmates in the ant Lasius niger , 2011, Insectes Sociaux.

[98]  F. Ratnieks,et al.  Synergy between social and private information increases foraging efficiency in ants , 2011, Biology Letters.

[99]  D. Sumpter,et al.  Optimisation in a natural system: Argentine ants solve the Towers of Hanoi , 2011, Journal of Experimental Biology.

[100]  Thomas D. Seeley,et al.  Honey bees use social information in waggle dances more fully when foraging errors are more costly , 2012 .

[101]  F. Ratnieks,et al.  Uncovering the complexity of ant foraging trails , 2012, Communicative & integrative biology.

[102]  David J. T. Sumpter,et al.  Individual Rules for Trail Pattern Formation in Argentine Ants (Linepithema humile) , 2012, PLoS Comput. Biol..

[103]  A. Cronin Consensus decision making in the ant Myrmecina nipponica: house-hunters combine pheromone trails with quorum responses , 2012, Animal Behaviour.

[104]  Boris Granovskiy,et al.  How dancing honey bees keep track of changes: the role of inspector bees , 2012 .

[105]  Klaus Jaffe,et al.  Chemical Recruitment for Foraging in Ants (Formicidae) and Termites (Isoptera): A Revealing Comparison , 2012 .

[106]  F. Ratnieks,et al.  Negative Feedback Enables Fast and Flexible Collective Decision-Making in Ants , 2012, PloS one.

[107]  Francis L. W. Ratnieks,et al.  Pheromone trails in the Brazilian ant Pheidole oxyops: extreme properties and dual recruitment action , 2012, Behavioral Ecology and Sociobiology.

[108]  Better the nest site you know: decision-making during nest migrations by the Pharaoh’s ant , 2012, Behavioral Ecology and Sociobiology.

[109]  S. Jarau,et al.  Learnt information in species-specific ‘trail pheromone’ communication in stingless bees , 2013, Animal Behaviour.

[110]  Nicola J. R. Plowes,et al.  Foraging behavior in the ant genus Messor (Hymenoptera: Formicidae: Myrmicinae) , 2013 .

[111]  Christoph Grüter,et al.  Negative feedback in ants: crowding results in less trail pheromone deposition , 2013, Journal of The Royal Society Interface.

[112]  M. Cammaerts Trail following Learning by Young Myrmica rubra Workers (Hymenoptera, Formicidae) , 2013 .

[113]  F. Ratnieks,et al.  Ant foraging on complex trails: route learning and the role of trail pheromones in Lasius niger , 2013, Journal of Experimental Biology.

[114]  Francis L. W. Ratnieks,et al.  Social learning strategies in honeybee foragers: do the costs of using private information affect the use of social information? , 2013, Animal Behaviour.

[115]  F. Ratnieks,et al.  Prey escorting behavior and possible convergent evolution of foraging recruitment mechanisms in an invasive ant , 2013 .

[116]  M. Beekman,et al.  Keeping track of changes: the performance of ant colonies in dynamic environments , 2013, Animal Behaviour.

[117]  Deborah M. Gordon,et al.  Fast and Flexible: Argentine Ants Recruit from Nearby Trails , 2013, PloS one.

[118]  M. Giurfa,et al.  Conceptual learning by miniature brains , 2013, Proceedings of the Royal Society B: Biological Sciences.

[119]  Richard Stafford,et al.  Snails and their trails: the multiple functions of trail‐following in gastropods , 2013, Biological reviews of the Cambridge Philosophical Society.

[120]  Tomer J Czaczkes,et al.  Effect of Trail Bifurcation Asymmetry and Pheromone Presence or Absence on Trail Choice by Lasius niger Ants , 2014, Ethology : formerly Zeitschrift fur Tierpsychologie.

[121]  C. Grüter,et al.  Insights from insects about adaptive social information use. , 2014, Trends in ecology & evolution.

[122]  Tomer J. Czaczkes,et al.  Ants use directionless odour cues to recall odour-associated locations , 2014, Behavioral Ecology and Sociobiology.

[123]  K. Akre,et al.  Psychophysics and the evolution of behavior. , 2014, Trends in ecology & evolution.

[124]  Dong-Hwan Choe,et al.  Pheromone communication in ants: a detailed analysis of concentration-dependent decisions in three species , 2014, Behavioral Ecology and Sociobiology.