Negative Feedback Enables Fast and Flexible Collective Decision-Making in Ants

Positive feedback plays a major role in the emergence of many collective animal behaviours. In many ants pheromone trails recruit and direct nestmate foragers to food sources. The strong positive feedback caused by trail pheromones allows fast collective responses but can compromise flexibility. Previous laboratory experiments have shown that when the environment changes, colonies are often unable to reallocate their foragers to a more rewarding food source. Here we show both experimentally, using colonies of Lasius niger, and with an agent-based simulation model, that negative feedback caused by crowding at feeding sites allows ant colonies to maintain foraging flexibility even with strong recruitment to food sources. In a constant environment, negative feedback prevents the frequently found bias towards one feeder (symmetry breaking) and leads to equal distribution of foragers. In a changing environment, negative feedback allows a colony to quickly reallocate the majority of its foragers to a superior food patch that becomes available when foraging at an inferior patch is already well underway. The model confirms these experimental findings and shows that the ability of colonies to switch to a superior food source does not require the decay of trail pheromones. Our results help to resolve inconsistencies between collective foraging patterns seen in laboratory studies and observations in the wild, and show that the simultaneous action of negative and positive feedback is important for efficient foraging in mass-recruiting insect colonies.

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

[2]  J. Deneubourg,et al.  Probabilistic behaviour in ants: A strategy of errors? , 1983 .

[3]  William J. Bell,et al.  Chemical Ecology of Insects , 1985, Springer US.

[4]  H. Dreisig Foraging rate of ants collecting honeydew or extrafloral nectar, and some possible constraints , 1988 .

[5]  R. Morse The Dance Language and Orientation of Bees , 1994 .

[6]  T. Seeley The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies , 1995 .

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

[8]  E. Bonabeau,et al.  Self-organization in social insects. , 1997, Trends in ecology & evolution.

[9]  Robinson,et al.  Self-organized criticality in termite architecture: a role for crowding in ensuring ordered nest expansion , 1999, Journal of theoretical biology.

[10]  K. Hoffmann,et al.  Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences , 1999, Oecologia.

[11]  Jean-Louis Deneubourg,et al.  Regulation of ants' foraging to resource productivity , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Paul Graham,et al.  Route learning by insects , 2003, Current Opinion in Neurobiology.

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

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

[15]  Dirk Helbing,et al.  Optimal traffic organization in ants under crowded conditions , 2004, Nature.

[16]  J. Deneubourg,et al.  Discrete dragline attachment induces aggregation in spiderlings of a solitary species , 2004, Animal Behaviour.

[17]  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.

[18]  J. Deneubourg,et al.  Experimental study and modelling of food recruitment in the antTetramorium impurum (Hym. Form.) , 1983, Insectes Sociaux.

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

[20]  Jean-Louis Deneubourg,et al.  Triggering and persistence of trail-laying in foragers of the ant Lasius niger. , 2005, Journal of insect physiology.

[21]  D. Sumpter The principles of collective animal behaviour , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

[24]  V. M. Schmidt,et al.  Collective foraging in a stingless bee: dependence on food profitability and sequence of discovery , 2006, Animal Behaviour.

[25]  José Halloy,et al.  Collegial decision making based on social amplification leads to optimal group formation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Joseph J. Hale,et al.  From Disorder to Order in Marching Locusts , 2006, Science.

[27]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[28]  F Mondada,et al.  Social Integration of Robots into Groups of Cockroaches to Control Self-Organized Choices , 2007, Science.

[29]  Markus Knaden,et al.  Smells like home: Desert ants, Cataglyphis fortis, use olfactory landmarks to pinpoint the nest , 2009, Frontiers in Zoology.

[30]  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.

[31]  F. Ratnieks,et al.  Combined use of pheromone trails and visual landmarks by the common garden ant Lasius niger , 2008, Behavioral Ecology and Sociobiology.

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

[33]  T. Oliver,et al.  Macroevolutionary patterns in the origin of mutualisms involving ants , 2008, Journal of evolutionary biology.

[34]  J. Deneubourg,et al.  Collective Decision-Making and Foraging Patterns in Ants and Honeybees , 2008 .

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

[36]  M. Collett Spatial memories in insects , 2009, Current Biology.

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

[38]  JEAN-LOUIS DENEUBOURG,et al.  Positive Feedback, Convergent Collective Patterns, and Social Transitions in Arthropods , 2009, Organization of Insect Societies.

[39]  Aaron Christ,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[40]  I. Couzin Collective cognition in animal groups , 2009, Trends in Cognitive Sciences.

[41]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[42]  J. Nieh A Negative Feedback Signal That Is Triggered by Peril Curbs Honey Bee Recruitment , 2010, Current Biology.

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

[44]  H. Swinney,et al.  Collective motion and density fluctuations in bacterial colonies , 2010, Proceedings of the National Academy of Sciences.

[45]  Leah Edelstein-Keshet,et al.  Inferring individual rules from collective behavior , 2010, Proceedings of the National Academy of Sciences.

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

[47]  I. Giardina Collective Animal Behavior David J.T. Sumpter Collective Animal Behavior , 2011, Animal Behaviour.

[48]  F. Ratnieks Honeybee Democracy Thomas D. Seeley Honeybee Democracy , 2011, Animal Behaviour.

[49]  V. Isaeva Self-organization in biological systems , 2012, Biology Bulletin.

[50]  Thomas Schlegel,et al.  Stop Signals Provide Cross Inhibition in Collective Decision-making , 2022 .

[51]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .