Dimensions of cognition in an insect, the honeybee.

This review provides evidence for the enormous richness of insect behavior, its high flexibility, and the cross-talk between different behavioral routines. The memory structure established by multiple forms of learning represents sensory inputs and relates behaviors in such a way that representations of complex environmental conditions are formed. Navigation and communication in social hymenoptera are particularly telling examples in this respect, but it is fair to conclude that similar integrated forms of dealing with the environment will be found in other insects when they are studied more closely. In this sense, research addressing behavioral complexity and its underlying neural substrates is necessary to characterize the real potential of insect learning and memory. Usually, such an approach has been used to characterize behavioral simplicity rather than complexity. It seems therefore timely to focus on the latter by studying problem solving alongside and in addition to elemental forms of learning.

[1]  Roland Maurer,et al.  Resetting the path integrator: a basic condition for route-based navigation , 2004, Journal of Experimental Biology.

[2]  K. Frisch The role of dances in recruiting bees to familiar sites , 1968 .

[3]  M. Srinivasan,et al.  The concepts of ‘sameness’ and ‘difference’ in an insect , 2001, Nature.

[4]  T. Seeley,et al.  Worker piping in honey bee swarms and its role in preparing for liftoff , 2001, Journal of Comparative Physiology A.

[5]  Thomas S Collett,et al.  Learning speed and contextual isolation in bumblebees. , 2002, The Journal of experimental biology.

[6]  G. Horridge,et al.  Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars. , 1997, Journal of insect physiology.

[7]  C. Thinus-Blanc The Cognitive Map Concept and its Consequences , 1987 .

[8]  A. S. Edwards,et al.  Ontogeny of orientation flight in the honeybee revealed by harmonic radar , 2000, Nature.

[9]  R. Menzel,et al.  Two spatial memories for honeybee navigation , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  Koehler ber die ?Sprache? der Bienen: Eine tierpsychologische Untersuchung , 1923 .

[11]  Thomas Seeley,et al.  Measurement of nest cavity volume by the honey bee (Apis mellifera) , 1977, Behavioral Ecology and Sociobiology.

[12]  Martin Fieder,et al.  Categorical learning in pigeons: the role of texture and shape in complex static stimuli , 1999, Vision Research.

[13]  C. D. L. Wynne,et al.  Deductive reasoning in pigeons , 1990, Naturwissenschaften.

[14]  C. Thinus-Blanc,et al.  Cognitive Processes and Spatial Orientation in Animal and Man , 1987 .

[15]  R. Menzel,et al.  Honey bees navigate according to a map-like spatial memory. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Andrew Pomiankowski,et al.  Symmetry is in the eye of the beholder. , 1994, Trends in ecology & evolution.

[17]  J. H. van Hateren,et al.  Pattern recognition in bees: orientation discrimination , 1990, Journal of Comparative Physiology A.

[18]  Scott Camazine,et al.  Collective decisions and cognition in bees , 1999, Nature.

[19]  Mandyam V Srinivasan,et al.  Visual working memory in decision making by honey bees. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Herbert S. Terrace,et al.  Memory and Representation of Serial Order by Children, Monkeys, and Pigeons , 1994 .

[21]  N. Mackintosh A Theory of Attention: Variations in the Associability of Stimuli with Reinforcement , 1975 .

[22]  K. Cheng,et al.  Honeybees (Apis mellifera) holding on to memories: response competition causes retroactive interference effects , 2006, Animal Cognition.

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

[24]  P. H. Wells,et al.  Do Honey Bees have a Language? , 1973, Nature.

[25]  A. Dickinson,et al.  Prometheus to Proust: the case for behavioural criteria for ‘mental time travel’ , 2003, Trends in Cognitive Sciences.

[26]  Fred C. Dyer,et al.  Motivation and vector navigation in honey bees , 2002, Naturwissenschaften.

[27]  Rüdiger Wehner,et al.  Idiosyncratic route-based memories in desert ants, Melophorus bagoti: How do they interact with path-integration vectors? , 2005, Neurobiology of Learning and Memory.

[28]  T. Seeley,et al.  Quorum sensing during nest-site selection by honeybee swarms , 2004, Behavioral Ecology and Sociobiology.

[29]  José Luis Bermúdez,et al.  Thinking Without Words , 2007 .

[30]  M. Srinivasan,et al.  Honeybee Odometry: Performance in Varying Natural Terrain , 2004, PLoS biology.

[31]  C. Freksa,et al.  Spatial Cognition, An Interdisciplinary Approach to Representing and Processing Spatial Knowledge , 1998 .

[32]  T. Collett,et al.  Insect navigation en route to the goal: multiple strategies for the use of landmarks , 1996, The Journal of experimental biology.

[33]  Hanspeter A. Mallot,et al.  Navigation and Acquisition of Spatial Knowledge in a Virtual Maze , 1998, Journal of Cognitive Neuroscience.

[34]  R. Menzel,et al.  Symmetry perception in an insect , 1996, Nature.

[35]  F. Huntingford Animal Thinking, Donald R. Griffin. Harvard University Press, Cambridge, Massachusetts (1984), ix, +237., Price £6.75 (paperback) , 1986 .

[36]  R. Menzel,et al.  Do insects have cognitive maps? , 1990, Annual review of neuroscience.

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

[38]  Roberta L. Klatzky,et al.  Allocentric and Egocentric Spatial Representations: Definitions, Distinctions, and Interconnections , 1998, Spatial Cognition.

[39]  T. Seeley,et al.  Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making , 2003, Behavioral Ecology and Sociobiology.

[40]  Lars Chittka,et al.  Can honey bees count landmarks? , 1995, Animal Behaviour.

[41]  O. Güntürkün Avian and mammalian “prefrontal cortices”: Limited degrees of freedom in the evolution of the neural mechanisms of goal-state maintenance , 2005, Brain Research Bulletin.

[42]  L. Tinbergen The Natural Control of Insects in Pinewoods , 1960 .

[43]  F. Dyer The biology of the dance language. , 2002, Annual review of entomology.

[44]  Guy Theraulaz,et al.  Nest excavation in ants: group size effects on the size and structure of tunneling networks , 2004, Naturwissenschaften.

[45]  R. Menzel,et al.  Colour preferences of flower-naive honeybees , 1995, Journal of Comparative Physiology A.

[46]  A. Bennett,et al.  Do animals have cognitive maps? , 1996, The Journal of experimental biology.

[47]  S. Harnad Categorical Perception: The Groundwork of Cognition , 1990 .

[48]  N. Mackintosh SELECTIVE ATTENTION IN ANIMAL DISCRIMINATION LEARNING. , 1965, Psychological bulletin.

[49]  F. Dyer 5 – Spatial Cognition: Lessons from Central-place Foraging Insects , 1998 .

[50]  F. Dyer Bees acquire route-based memories but not cognitive maps in a familiar landscape , 1991, Animal Behaviour.

[51]  Matthew Collett,et al.  Path integration in insects , 2000, Current Opinion in Neurobiology.

[52]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[53]  Mandyam V. Srinivasan,et al.  Grouping of visual objects by honeybees , 2004, Journal of Experimental Biology.

[54]  R. Menzel,et al.  Bees travel novel homeward routes by integrating separately acquired vector memories , 1998, Animal Behaviour.

[55]  B. Ronacher,et al.  Desert ants Cataglyphis fortis use self-induced optic flow to measure distances travelled , 1995, Journal of Comparative Physiology A.

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

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

[58]  Paul Graham,et al.  View-based navigation in insects: how wood ants (Formica rufa L.) look at and are guided by extended landmarks. , 2002, The Journal of experimental biology.

[59]  M. Lindauer Schwarmbienen auf Wohnungssuche , 1955, Zeitschrift für vergleichende Physiologie.

[60]  Esch,et al.  Distance estimation by foraging honeybees , 1996, The Journal of experimental biology.

[61]  J. Delius,et al.  Stimulus equivalencies through discrimination reversals , 2000 .

[62]  Zhang,et al.  Visually mediated odometry in honeybees , 1997, The Journal of experimental biology.

[63]  T. Seeley,et al.  Modeling and analysis of nest-site selection by honeybee swarms: the speed and accuracy trade-off , 2005, Behavioral Ecology and Sociobiology.

[64]  M. Giurfa,et al.  A test of transitive inferences in free-flying honeybees: unsuccessful performance due to memory constraints. , 2004, Learning & memory.

[65]  P. Visscher,et al.  House-hunting by honey bee swarms: collective decisions and individual behaviors , 1999, Insectes Sociaux.

[66]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

[67]  Randolf Menzel,et al.  Encoding spatial information in the waggle dance , 2005, Journal of Experimental Biology.

[68]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[69]  Isabelle Pastergue-Ruiz,et al.  Can the antCataglyphis cursor (Hymenoptera: Formicidae) encode global landmark-landmark relationships in addition to isolated landmark-goal relationships? , 2005, Journal of Insect Behavior.

[70]  Thomas S Collett,et al.  The use of landmarks and panoramic context in the performance of local vectors by navigating honeybees. , 2002, The Journal of experimental biology.

[71]  M. Giurfa,et al.  Vectors, routes and maps: new discoveries about navigation in insects , 1999, Trends in Neurosciences.

[72]  Martin Giurfa,et al.  Symmetry is in the eye of the ‘beeholder’: innate preference for bilateral symmetry in flower-naïve bumblebees , 2004, Naturwissenschaften.

[73]  M. Scheerer,et al.  Problem Solving , 1967, Nature.

[74]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[75]  Jürgen Tautz,et al.  One-strided waggle dance in bees , 1996, Nature.

[76]  N. Schmajuk,et al.  Occasion setting: Associative learning and cognition in animals. , 1998 .

[77]  L. Tinbergen The natural control of insects in pinewoods. I. Factors influencing the intensity of predation by songbirds , 1960 .

[78]  R. Wehner,et al.  Ant Navigation: One-Way Routes Rather Than Maps , 2006, Current Biology.

[79]  S. Al-Moghrabi,et al.  Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake , 1996 .

[80]  B. Katz Action potentials from a sensory nerve ending , 1950, The Journal of physiology.

[81]  B. Katz,et al.  Depolarization of sensory terminals and the initiation of impulses in the muscle spindle , 1950, The Journal of physiology.

[82]  David Premack,et al.  The Mind of an Ape , 1983 .

[83]  D. Griffin,et al.  New evidence of animal consciousness , 2003, Animal Cognition.

[84]  M. Lindauer,et al.  Sonnenorientierung der Bienen unter der Äquatorsonne und zur Nachtzeit , 2004, Naturwissenschaften.

[85]  R. Menzel,et al.  The flight paths of honeybees recruited by the waggle dance , 2005, Nature.

[86]  H. Esch,et al.  Honeybees use optic flow to measure the distance of a food source , 2005, Naturwissenschaften.

[87]  R W GERARD,et al.  Membrane potentials and excitation of impaled single muscle fibers. , 1946, Journal of cellular and comparative physiology.

[88]  A. Gumbert Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning , 2000, Behavioral Ecology and Sociobiology.

[89]  J. L. Gould,et al.  Honey Bee Orientation: A Backup System for Cloudy Days , 1981, Science.

[90]  R. Wehner,et al.  Visual navigation in insects: coupling of egocentric and geocentric information , 1996, The Journal of experimental biology.

[91]  A. Wenner,et al.  Recruitment Efficiency in Honeybees: Studies on the Role of Olfaction , 1970 .

[92]  M V Srinivasan,et al.  Honeybee navigation: nature and calibration of the "odometer". , 2000, Science.

[93]  N. Emery Cognitive ornithology: the evolution of avian intelligence , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[94]  Martin Giurfa,et al.  Conditioning procedure and color discrimination in the honeybee Apis mellifera , 2004, Naturwissenschaften.

[95]  G. Roth,et al.  Brain Evolution and Cognition , 2000 .

[96]  M. Hammer,et al.  Pattern learning by honeybees: conditioning procedure and recognition strategy , 1999, Animal Behaviour.

[97]  Thomas S. Collett,et al.  Rapid Navigational Learning in Insects with a Short Lifespan , 1998, Connect. Sci..

[98]  G. Beugnon,et al.  Vision-independent odometry in the ant Cataglyphis cursor , 2005, Naturwissenschaften.

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

[100]  T. Seeley,et al.  Group decision making in swarms of honey bees , 1999, Behavioral Ecology and Sociobiology.

[101]  C. Allen,et al.  The Cognitive Animal: Empirical and Theoretical Perspectives on Animal Cognition , 2002 .

[102]  T. Zentall,et al.  Categorization, concept learning, and behavior analysis: an introduction. , 2002, Journal of the experimental analysis of behavior.

[103]  J. Hildebrand,et al.  Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta , 1989, Cell and Tissue Research.

[104]  Friedrich Otto,et al.  Die Bedeutung des Rückfluges für die Richtungs- und Entfernungsangabe der Bienen , 1959, Zeitschrift für vergleichende Physiologie.

[105]  C. Gallistel The organization of learning , 1990 .

[106]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[107]  Koehler Über die „Sprache“ der Bienen , 1923, Naturwissenschaften.

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

[109]  M. Giurfa Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain , 2003, Current Opinion in Neurobiology.

[110]  M. Srinivasan,et al.  Maze Learning by Honeybees , 1996, Neurobiology of Learning and Memory.

[111]  T. McNamara,et al.  Multiple views of spatial memory , 1997 .

[112]  Martin Giurfa,et al.  Local-feature assembling in visual pattern recognition and generalization in honeybees , 2004, Nature.

[113]  K. Takeda Classical conditioned response in the honey bee , 1961 .

[114]  T. Zentall Selective and divided attention in animals , 2005, Behavioural Processes.