Individual versus collective cognition in social insects

ABSTRACT The concerted responses of eusocial insects to environmental stimuli are often referred to as collective cognition at the level of the colony. To achieve collective cognition, a group can draw on two different sources: individual cognition and the connectivity between individuals. Computation in neural networks, for example, is attributed more to sophisticated communication schemes than to the complexity of individual neurons. The case of social insects, however, can be expected to differ. This is because individual insects are cognitively capable units that are often able to process information that is directly relevant at the level of the colony. Furthermore, involved communication patterns seem difficult to implement in a group of insects as they lack a clear network structure. This review discusses links between the cognition of an individual insect and that of the colony. We provide examples for collective cognition whose sources span the full spectrum between amplification of individual insect cognition and emergent group-level processes. Summary: This Review discusses how social insect colonies draw on both the cognition of their individual members and the interaction networks between these individuals to form collective cognition.

[1]  Amos Korman,et al.  A locally-blazed ant trail achieves efficient collective navigation despite limited information , 2016, eLife.

[2]  Ofer Feinerman,et al.  Social brains and behavior: past and present , 2016 .

[3]  J. Witte The Ants , 2016 .

[4]  Guy Theraulaz,et al.  Stigmergic construction and topochemical information shape ant nest architecture , 2016, Proceedings of the National Academy of Sciences.

[5]  T. O. Richardson,et al.  Beyond contact-based transmission networks: the role of spatial coincidence , 2015, Journal of The Royal Society Interface.

[6]  J. Cvačka,et al.  Complex alarm strategy in the most basal termite species , 2015, Behavioral Ecology and Sociobiology.

[7]  Hunter King,et al.  Termite mounds harness diurnal temperature oscillations for ventilation , 2015, Proceedings of the National Academy of Sciences.

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

[9]  Ofer Feinerman,et al.  Ant groups optimally amplify the effect of transiently informed individuals , 2015, Nature Communications.

[10]  Daniel Polani,et al.  An Informational Study of the Evolution of Codes and of Emerging Concepts in Populations of Agents , 2015, Artificial Life.

[11]  Jacek Szwedo,et al.  Brood care in a 100-million-year-old scale insect , 2015, eLife.

[12]  Amos Korman,et al.  Confidence Sharing: An Economic Strategy for Efficient Information Flows in Animal Groups , 2014, PLoS Comput. Biol..

[13]  E. Robinson,et al.  How collective comparisons emerge without individual comparisons of the options , 2014, Proceedings of the Royal Society B: Biological Sciences.

[14]  Úna C. Farrell,et al.  Exceptionally Preserved 450-Million-Year-Old Ordovician Ostracods with Brood Care , 2014, Current Biology.

[15]  Bernhard Haeupler,et al.  Breathe before speaking: efficient information dissemination despite noisy, limited and anonymous communication , 2013, Distributed Computing.

[16]  Antoine Wystrach,et al.  Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit , 2013, Proceedings of the Royal Society B: Biological Sciences.

[17]  S. Pratt,et al.  Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy , 2013, Proceedings of the National Academy of Sciences.

[18]  A. Crespi,et al.  Tracking Individuals Shows Spatial Fidelity Is a Key Regulator of Ant Social Organization , 2013, Science.

[19]  Jean-Pierre Eckmann,et al.  Desert ants achieve reliable recruitment across noisy interactions , 2013, Journal of The Royal Society Interface.

[20]  Deborah M. Gordon,et al.  Interactions with Combined Chemical Cues Inform Harvester Ant Foragers' Decisions to Leave the Nest in Search of Food , 2013, PloS one.

[21]  Xiaoya Ma,et al.  Complex brain and optic lobes in an early Cambrian arthropod , 2012, Nature.

[22]  S. Pratt,et al.  Groups have a larger cognitive capacity than individuals , 2012, Current Biology.

[23]  Ofer Feinerman,et al.  Experience, corpulence and decision making in ant foraging , 2012, Journal of Experimental Biology.

[24]  Amos Korman,et al.  Memory Lower Bounds for Randomized Collaborative Search and Implications for Biology , 2012, DISC.

[25]  T. Seeley,et al.  Stop Signals Provide Cross Inhibition in Collective Decision-Making by Honeybee Swarms , 2012, Science.

[26]  L. Giraldeau,et al.  Exploring the Costs and Benefits of Social Information Use , 2011 .

[27]  Deborah M. Gordon,et al.  The effect of individual variation on the structure and function of interaction networks in harvester ants , 2011, Journal of The Royal Society Interface.

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

[29]  Michael B. Reiser,et al.  Visual Place Learning in Drosophila melanogaster , 2011, Nature.

[30]  M. Elgar,et al.  Evolution of cuticular hydrocarbon diversity in ants , 2011, Journal of evolutionary biology.

[31]  Samuel Ellis,et al.  A Simple Threshold Rule Is Sufficient to Explain Sophisticated Collective Decision-Making , 2011, PloS one.

[32]  Anna Dornhaus,et al.  Time-Ordered Networks Reveal Limitations to Information Flow in Ant Colonies , 2011, PloS one.

[33]  T. O. Richardson,et al.  Ants in a Labyrinth: A Statistical Mechanics Approach to the Division of Labour , 2011, PloS one.

[34]  S. Farris,et al.  Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects , 2011, Proceedings of the Royal Society B: Biological Sciences.

[35]  S. Pratt,et al.  Emergence of group rationality from irrational individuals , 2011 .

[36]  Correction for Ward et al., Fast and accurate decisions through collective vigilance in fish shoals , 2011, Proceedings of the National Academy of Sciences.

[37]  Douglas Blackiston,et al.  Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae) , 2011, Journal of Experimental Biology.

[38]  D. Sumpter,et al.  Fast and accurate decisions through collective vigilance in fish shoals , 2011, Proceedings of the National Academy of Sciences.

[39]  G. Latil,et al.  Use of radio-tagging to map spatial organization and social interactions in insects , 2011, Journal of Experimental Biology.

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

[41]  Robin I. M. Dunbar,et al.  Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality , 2010, Proceedings of the National Academy of Sciences.

[42]  James S. Waters,et al.  Allometric Scaling of Metabolism, Growth, and Activity in Whole Colonies of the Seed‐Harvester Ant Pogonomyrmex californicus , 2010, The American Naturalist.

[43]  M. Kaspari,et al.  Energetic basis of colonial living in social insects , 2010, Proceedings of the National Academy of Sciences.

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

[45]  X. Cerdá,et al.  Cooperative prey-retrieving in the ant Cataglyphis floricola: an unusual short-distance recruitment , 2010, Insectes Sociaux.

[46]  Nigel R Franks,et al.  Flexible task allocation and the organization of work in ants , 2009, Proceedings of the Royal Society B: Biological Sciences.

[47]  J. Niven,et al.  Are Bigger Brains Better? , 2009, Current Biology.

[48]  S. Martin,et al.  A Review of Ant Cuticular Hydrocarbons , 2009, Journal of Chemical Ecology.

[49]  S. Pratt,et al.  Rationality in collective decision-making by ant colonies , 2009, Proceedings of the Royal Society B: Biological Sciences.

[50]  Omer Reingold,et al.  How Well Do Random Walks Parallelize? , 2009, APPROX-RANDOM.

[51]  S. Behmer,et al.  Animal Behaviour: Feeding the Superorganism , 2009, Current Biology.

[52]  Anthony Raw,et al.  The biology of the solitary bee Osmia rufa (L.) (Megachilidae) , 2009 .

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

[54]  Anna Dornhaus,et al.  Spatial organization and division of labour in the bumblebee Bombus impatiens , 2009, Animal Behaviour.

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

[56]  T. O. Richardson,et al.  Radio tagging reveals the roles of corpulence, experience and social information in ant decision making , 2009, Behavioral Ecology and Sociobiology.

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

[58]  E. Wilson,et al.  The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies , 2008 .

[59]  B. Dickson Wired for Sex: The Neurobiology of Drosophila Mating Decisions , 2008, Science.

[60]  Kevin M Schultz,et al.  The mechanism of flight guidance in honeybee swarms: subtle guides or streaker bees? , 2008, Journal of Experimental Biology.

[61]  Noga Alon,et al.  Many random walks are faster than one , 2007, SPAA '08.

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

[63]  Brian L. Fisher,et al.  Evaluating alternative hypotheses for the early evolution and diversification of ants , 2006, Proceedings of the National Academy of Sciences.

[64]  D. Sumpter,et al.  From Compromise to Leadership in Pigeon Homing , 2006, Current Biology.

[65]  C. Moreau,et al.  Phylogeny of the Ants: Diversification in the Age of Angiosperms , 2006, Science.

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

[67]  Eamonn B. Mallon,et al.  An agent-based model of collective nest choice by the ant Temnothorax albipennis , 2005, Animal Behaviour.

[68]  Andrew M Simons,et al.  Many wrongs: the advantage of group navigation. , 2004, Trends in ecology & evolution.

[69]  S. Graham,et al.  Honey Bee Nest Thermoregulation: Diversity Promotes Stability , 2004, Science.

[70]  Walter R. Tschinkel,et al.  The nest architecture of the Florida harvester ant, Pogonomyrmex badius , 2004, Journal of insect science.

[71]  J. Fewell Social Insect Networks , 2003, Science.

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

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

[74]  R. Wehner Desert ant navigation: how miniature brains solve complex tasks , 2003, Journal of Comparative Physiology A.

[75]  Guy Theraulaz,et al.  The formation of spatial patterns in social insects: from simple behaviours to complex structures , 2003, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[76]  Eric J. Warrant,et al.  Visual cues used by ball-rolling dung beetles for orientation , 2003, Journal of Comparative Physiology A.

[77]  Pekka Orponen,et al.  Continuous-Time Symmetric Hopfield Nets Are Computationally Universal , 2003, Neural Computation.

[78]  Eamonn B. Mallon,et al.  Strategies for choosing between alternatives with different attributes: exemplified by house-hunting ants , 2003, Animal Behaviour.

[79]  Eamonn B. Mallon,et al.  Information flow, opinion polling and collective intelligence in house-hunting social insects. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[80]  Achim Gathmann,et al.  Foraging ranges of solitary bees , 2002 .

[81]  E. Tibbetts Visual signals of individual identity in the wasp Polistes fuscatus , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[82]  S. Robson,et al.  Transient division of labor and behavioral specialization in the ant Formica schaufussi , 2002, Naturwissenschaften.

[83]  Shaowu Zhang,et al.  Honeybee dances communicate distances measured by optic flow , 2001, Nature.

[84]  D. McShea,et al.  Individual versus social complexity, with particular reference to ant colonies , 2001, Biological reviews of the Cambridge Philosophical Society.

[85]  Kevin M. O'Neill,et al.  Solitary Wasps: Behavior and Natural History , 2001 .

[86]  Thomas S. Collett,et al.  How do insects use path integration for their navigation? , 2000, Biological Cybernetics.

[87]  Thomas D. Seeley,et al.  Fever in honeybee colonies , 2000, Naturwissenschaften.

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

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

[90]  Guy Theraulaz,et al.  A Brief History of Stigmergy , 1999, Artificial Life.

[91]  J. Strassmann,et al.  KIN SELECTION AND SOCIAL INSECTS , 1998 .

[92]  NIGEL R FRANKS,et al.  Self-organizing nest construction in ants: individual worker behaviour and the nest's dynamics , 1997, Animal Behaviour.

[93]  E. Bonabeau,et al.  Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[94]  Deborah M. Gordon,et al.  The expandable network of ant exploration , 1995, Animal Behaviour.

[95]  T. Seeley The Wisdom of the Hive , 1995 .

[96]  N. Franks,et al.  Spatial relationships within nests of the ant Leptothorax unifasciatus (Latr.) and their implications for the division of labour , 1995, Animal Behaviour.

[97]  L. Aiello,et al.  The Expensive-Tissue Hypothesis: The Brain and the Digestive System in Human and Primate Evolution , 1995, Current Anthropology.

[98]  Bernard J. Crespi,et al.  The definition of eusociality , 1995 .

[99]  N. Franks,et al.  Foraging for work: how tasks allocate workers , 1994, Animal Behaviour.

[100]  F. Roces,et al.  Stridulation in leaf-cutting ants , 1993, Naturwissenschaften.

[101]  D. Gordon,et al.  What is the function of encounter patterns in ant colonies? , 1993, Animal Behaviour.

[102]  Scott Camazine,et al.  The regulation of pollen foraging by honey bees: how foragers assess the colony's need for pollen , 1993, Behavioral Ecology and Sociobiology.

[103]  S. N. Fry,et al.  Sequence learning by honeybees , 1993, Journal of Comparative Physiology A.

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

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

[106]  E. Bernays,et al.  Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators , 1991 .

[107]  K. Jaffe,et al.  Orientation cues used by ants , 1990, Insectes Sociaux.

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

[109]  N. Franks Army Ants: A Collective Intelligence , 1989 .

[110]  E. Wilson,et al.  Dense heterarchies and mass communication as the basis of organization in ant colonies. , 1988, Trends in ecology & evolution.

[111]  J. L. Gould The Locale Map of Honey Bees: Do Insects Have Cognitive Maps? , 1986, Science.

[112]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Thomas D. Seeley,et al.  Colony Defense Strategies of the Honeybees in Thailand , 1982 .

[114]  H. Topoff,et al.  Avoiding predation by army ants: Defensive behaviours of three ant species of the genus Camponotus , 1981, Animal Behaviour.

[115]  D. F. Howard,et al.  The flow of food in colonies of the fire ant, Solenopsis invicta: a multifactorial study , 1981 .

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

[117]  P. Howse,et al.  The mass recruitment system of the leaf cutting ant, Atta cephalotes (L.) , 1979, Animal Behaviour.

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

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

[120]  P.-P. Grasse La reconstruction du nid et les coordinations interindividuelles chezBellicositermes natalensis etCubitermes sp. la théorie de la stigmergie: Essai d'interprétation du comportement des termites constructeurs , 1959, Insectes Sociaux.

[121]  M. Rockstein Bees. Their Vision, Chemical Senses, and Language , 1952 .

[122]  O. Feinerman,et al.  Social complexity, diet, and brain evolution: modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants , 2015, Behavioral Ecology and Sociobiology.

[123]  Tomer J. Czaczkes,et al.  Cooperative transport in ants (Hymenoptera: Formicidae) and elsewhere , 2013 .

[124]  Audrey Dussutour,et al.  How to tell your mates—costs and benefits of different recruitment mechanisms , 2009 .

[125]  Moshe Abeles,et al.  Synfire chains , 2009, Scholarpedia.

[126]  P. Visscher Group decision making in nest-site selection among social insects. , 2007, Annual review of entomology.

[127]  T. Seeley,et al.  Group decision making in honey bee swarms , 2006 .

[128]  G. J. Blomquist,et al.  Ecological, behavioral, and biochemical aspects of insect hydrocarbons. , 2005, Annual review of entomology.

[129]  Tom De Wolf,et al.  Emergence Versus Self-Organisation: Different Concepts but Promising When Combined , 2004, Engineering Self-Organising Systems.

[130]  Stephen Wolfram,et al.  A New Kind of Science , 2003, Artificial Life.

[131]  J. Fewell,et al.  Models of division of labor in social insects. , 2001, Annual review of entomology.

[132]  J. Darlington,et al.  Termite Nests: Architecture, Regulation and Defence , 2000 .

[133]  L. Brower,et al.  Monarch butterfly orientation: missing pieces of a magnificent puzzle , 1996, The Journal of experimental biology.

[134]  G. Robinson Regulation of division of labor in insect societies. , 1992, Annual review of entomology.

[135]  M. Abeles Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[136]  Mats G. Nordahl,et al.  Universal Computation in Simple One-Dimensional Cellular Automata , 1990, Complex Syst..

[137]  D. Evans,et al.  Book Reviews: Insect Defenses. Adaptive Mechanisms and Strategies of Prey and Predators. , 1990 .

[138]  J. Deneubourg,et al.  Colony size, communication and ant foraging strategy , 1989 .

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

[140]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[141]  T. Alloway Learning and Memory in Insects , 1972 .

[142]  Howard E. Evans,et al.  The Behavior Patterns of Solitary Wasps , 1966 .

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

[144]  E. Wilson Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith) 2. An information analysis of the odour trail , 1962 .

[145]  C. L. Stong,et al.  The amateur scientist. , 1960, Scientific American.

[146]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[147]  A. Emerson,et al.  Social Coordination and the Superorganism , 1939 .

[148]  Anna Dornhaus,et al.  Individual and collective cognition in ants and other insects ( Hymenoptera : Formicidae ) , 2008 .