Information synergy: adding unambiguous quality information rescues social information use in ants

Animals have access to many alternative information sources when making decisions, such as private information (e.g. memory) and social information. Social insects make extensive use of social information. However, when intentional social information (e.g. pheromone trails in ants) conflicts with private information (e.g. route memories), insects often follow their private information. Why is this? We propose that an asymmetry in the type of information provided by these two information sources drives the neglect of social information: In ants, workers with certain information about the quality of a food source (memory) ignore valuable social information (pheromone trails) because the pheromone trails encode only a very ambiguous measure of food quality. This leads to a testable hypothesis: the addition of unambiguous quality information should rescue social information following. To test this, we trained ants to a poor quality (0.25M sucrose) food source, and then provided an alternative path along with either 1) no information, 2) a pheromone trail, 3) a 0.2μl 1.5M sucrose droplet, providing unambiguous quality information, or 4) both a trail and a droplet. When either no or only one information source was provided (1-3), most ants (60-75%) continued following their own memory. However, the addition of unambiguous quality information (4) rescued trail following: when both a trail and a droplet were provided, 75% of ants followed the trail. In further experiments, we show that quality information gleaned from direct contact with fed nestmates produced similar effects. Using florescence microscopy, we demonstrate that food (and information) flows from fed workers to outgoing foragers, explaining the frequent contacts on trails. We propose that the type of information an information source can convey, and its ambiguity, is a strong driver of which source of information is attended to.

[1]  T. Czaczkes,et al.  Individual ant workers show self-control , 2017, Biology Letters.

[2]  Mandyam V Srinivasan,et al.  Floral scents induce recall of navigational and visual memories in honeybees , 2004, Journal of Experimental Biology.

[3]  Ofer Feinerman,et al.  Ant trophallactic networks: simultaneous measurement of interaction patterns and food dissemination , 2015, Scientific Reports.

[4]  M. Lihoreau,et al.  Commentary: Do Bees Play the Producer-Scrounger Game? , 2016, Front. Psychol..

[5]  K. Laland,et al.  The evolutionary basis of human social learning , 2012, Proceedings of the Royal Society B: Biological Sciences.

[6]  J. Keynes A Treatise on Probability. , 1923 .

[7]  N. Franks,et al.  Knowledgeable individuals lead collective decisions in ants , 2011, Journal of Experimental Biology.

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

[9]  E. Leadbeater,et al.  A social insect perspective on the evolution of social learning mechanisms , 2017, Proceedings of the National Academy of Sciences.

[10]  Ofer Feinerman,et al.  Individual crop loads provide local control for collective food intake in ant colonies , 2018, eLife.

[11]  How memory and motivation modulate the responses to trail pheromones in three ant species , 2016, Behavioral Ecology and Sociobiology.

[12]  R. Mann,et al.  Social and private information influence the decision making of Australian meat ants (Iridomyrmex purpureus) , 2018, Insectes Sociaux.

[13]  Anna Dornhaus,et al.  Who Are the "Lazy" Ants? The Function of Inactivity in Social Insects and a Possible Role of Constraint: Inactive Ants Are Corpulent and May Be Young and/or Selfish. , 2017, Integrative and comparative biology.

[14]  Kevin N Laland,et al.  Nine-spined sticklebacks exploit the most reliable source when public and private information conflict , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  Anna Dornhaus,et al.  Workers ‘specialized’ on inactivity: Behavioral consistency of inactive workers and their role in task allocation , 2015, Behavioral Ecology and Sociobiology.

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

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

[18]  I. Coolen,et al.  Trade‐Offs in the Adaptive Use of Social and Asocial Learning , 2005 .

[19]  Christopher D. Chambers,et al.  Redefine statistical significance , 2017, Nature Human Behaviour.

[20]  C. Grüter,et al.  Informational conflicts created by the waggle dance , 2008, Proceedings of the Royal Society B: Biological Sciences.

[21]  D. Mautz,et al.  Der Kommunikationseffekt der Schwänzeltänze bei Apis mellifica carnica (Pollm.) , 1971, Zeitschrift für vergleichende Physiologie.

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

[23]  Sarah R. Heilbronner,et al.  Ambiguity Aversion in Rhesus Macaques , 2010, Front. Neurosci..

[24]  T. Seeley,et al.  Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability , 2000, Journal of Comparative Physiology A.

[25]  Craig R. Fox,et al.  Ambiguity Aversion and Comparative Ignorance , 1995 .

[26]  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.

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

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

[29]  I. Coolen,et al.  Adaptive trade-offs in the use of social and personal information. , 2009 .

[30]  K. Laland,et al.  Social learning strategies and predation risk: minnows copy only when using private information would be costly , 2008, Proceedings of the Royal Society B: Biological Sciences.

[31]  W. Farina,et al.  Trophallaxis: A Mechanism of Information Transfer , 2009 .

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

[33]  K. Laland Social learning strategies , 2004, Learning & behavior.

[34]  James A. R. Marshall,et al.  Decision-making under uncertainty: biases and Bayesians , 2011, Animal Cognition.

[35]  J. Deneubourg,et al.  How do ants assess food volume? , 2000, Animal Behaviour.

[36]  B. Webb,et al.  Optimal cue integration in ants , 2015, Proceedings of the Royal Society B: Biological Sciences.

[37]  J. Clobert,et al.  Social information and emigration: lessons from immigrants. , 2007, Ecology letters.

[38]  G. Dreisbach,et al.  Voluntary Switching in an Invertebrate: The Effect of Cue and Reward Change , 2018, Journal of experimental psychology. Animal learning and cognition.

[39]  A. Dornhaus,et al.  Foraging Bumble Bees Weigh the Reliability of Personal and Social Information , 2016, Current Biology.

[40]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[41]  F. Knight The economic nature of the firm: From Risk, Uncertainty, and Profit , 2009 .

[42]  I. Coolen,et al.  Species difference in adaptive use of public information in sticklebacks , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  M. Gil,et al.  Olfactory learning by means of trophallaxis in Apis mellifera , 2005, Journal of Experimental Biology.

[44]  D. Ellsberg Decision, probability, and utility: Risk, ambiguity, and the Savage axioms , 1961 .

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

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

[47]  A. Tversky,et al.  Prospect theory: an analysis of decision under risk — Source link , 2007 .

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

[49]  Y. Provecho,et al.  Olfactory memory established during trophallaxis affects food search behaviour in ants , 2009, Journal of Experimental Biology.

[50]  Roxana Josens,et al.  Individual olfactory learning in Camponotus ants , 2006, Animal Behaviour.

[51]  T. Czaczkes,et al.  Relative value perception in an insect: positive and negative incentive contrasts in ants , 2018, bioRxiv.

[52]  I. Coolen,et al.  Social Learning in Noncolonial Insects? , 2005, Current Biology.

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

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

[55]  Yoram Halevy Ellsberg Revisited: An Experimental Study , 2005 .

[56]  Adam G. Hart,et al.  Why do honey-bee (Apis millifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system , 2001, Behavioral Ecology and Sociobiology.

[57]  Christoph Grüter,et al.  Social Learning: The Importance of Copying Others , 2010, Current Biology.

[58]  Richard James,et al.  Emergency networking: famine relief in ant colonies , 2010, Animal Behaviour.

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

[60]  Thierry Hoinville,et al.  Steering intermediate courses: desert ants combine information from various navigational routines , 2016, Journal of Comparative Physiology A.

[61]  Pheromone trail following in the ant Lasius niger: high accuracy and variability but no effect of task state , 2017 .

[62]  Sasha R. X. Dall,et al.  Information and its use by animals in evolutionary ecology. , 2005, Trends in ecology & evolution.

[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]  A. Tversky,et al.  Prospect theory: analysis of decision under risk , 1979 .

[65]  J. Pasteels,et al.  Spatial specialization of the foragers and foraging strategy inLasius fuliginosus (Latreille) (Hymenoptera, Formicidae) , 1996, Insectes Sociaux.

[66]  Ellouise Leadbeater,et al.  Foraging bumblebees do not rate social information above personal experience , 2014, Behavioral Ecology and Sociobiology.

[67]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[68]  Tamsyn H. Bridger,et al.  Ants show a leftward turning bias when exploring unknown nest sites , 2014, Biology Letters.

[69]  B. Hare,et al.  Chimpanzees and bonobos distinguish between risk and ambiguity , 2011, Biology Letters.

[70]  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.

[71]  T. Lillicrap,et al.  Why Copy Others? Insights from the Social Learning Strategies Tournament , 2010, Science.

[72]  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.

[73]  R. Josens,et al.  Food information acquired socially overrides individual food assessment in ants , 2016, Behavioral Ecology and Sociobiology.

[74]  Chemical trail systems, orientation, and territorial interactions in the antLasius neoniger , 1989, Journal of Insect Behavior.