Energetic cost of learning and memory can cause cognitive impairment in honeybees

Biology Letters

Volumn 9, Issue 4, 2013, Pages

  Jaumann, Sarah ^a   Scudelari, Robin ^a   Naug, Dhruba ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Cognition; Energetic stress; Honeybees; Learning; Memory; Trade off

Indexed keywords

BIOENERGETICS; COGNITION; COLONY; ENTOMOLOGY; HONEYBEE; LEARNING; LIFE HISTORY TRAIT; MEMORY; RESOURCE ALLOCATION; TRADE-OFF;

APIS MELLIFERA; APOIDEA;

ANIMAL; BEE; COGNITION; ENERGY METABOLISM; LEARNING; MEMORY; PHYSIOLOGY; ARTICLE; ENERGETIC STRESS; HONEYBEE; TRADE-OFF;

ANIMALS; ASSOCIATION LEARNING; BEES; COGNITION; ENERGY METABOLISM; MEMORY;

COGNITION; ENERGETIC STRESS; HONEYBEES; LEARNING; MEMORY; TRADE-OFF;

EID: 84880807609     PISSN: 17449561     EISSN: 1744957X     Source Type: Journal    
DOI: 10.1098/rsbl.2013.0149     Document Type: Article

References (19)

1. Ames A. 2000 CNS energy metabolism as related to function. Brain Res. Rev. 34, 42-68. (doi:10.1016/S0165-0173(00)00038-2).
2. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC. 1998 The metabolic cost of neural information. Nat. Neurosci. 1, 36-41. (doi:10. 1038/236). (Pubitemid 128652639)
3. Dukas R. 1999 Cost of memory: ideas and predictions. J. Theor. Biol. 197, 41-50. (doi:10. 1006/jtbi.1998.0856).
4. Mery F, Kawecki TJ. 2005 A cost of long-term memory in Drosophila. Science 308, 1148. (doi:10. 1126/science.1111331). (Pubitemid 40696428)
5. Snell-Rood EC, Davidowitz G, Papaj DR. 2011 Reproductive tradeoffs of learning in a butterfly. Behav. Ecol. 22, 291-302. (doi:10.1093/beheco/arq169).
6. Pravosudov VV, Lavenex P, Omanska A. 2005 Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav. Neurosci. 119, 1368-1374. (doi:10. 1037/0735-7044.119.5.1368). (Pubitemid 41598748)
7. Nowicki S, Searcy WA, Peters S. 2002 Brain development, song learning and mate choice in birds: A review and experimental test of the 'nutritional stress hypothesis'. J. Comp. Physiol. A 188, 1003-1014. (Pubitemid 36251493)
8. Mattila HR, Smith BH. 2008 Learning and memory in workers reared by nutritionally stressed honeybee (Apis mellifera L.) colonies. Physiol. Behav. 95, 609-616. (doi:10.1016/j.physbeh.2008.08.003).
9. Friedrich A, Thomas U, Müller U. 2004 Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J. Neurosci. 24, 4460-4468. (doi:10.1523/JNEUROSCI.0669-04.2004). (Pubitemid 38608157)
10. Mayack C, Naug D. 2010 Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J. Insect Physiol. 56, 1572-1575. (doi:10. 1016/j.jinsphys.2010.05.016).
11. Mallon EB, Brockmann A, Schmid-Hempel P. 2003 Immune response inhibits associative learning in insects. Proc. R. Soc. Lond. B 270, 2471-2473. (doi:10.1098/rspb.2003.2456). (Pubitemid 37500240)
12. Gegear RJ, Otterstatter MC, Thomson JD. 2006 Bumblebee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc. R. Soc. B 273, 1073-1078. (doi:10.1098/rspb.2005.3423). (Pubitemid 47324474)
13. Kralj J, Brockmann A, Fuchs S, Tautz J. 2007 The parasitic mite Varroa destructor affects nonassociative learning in honeybee foragers, Apismellifera L. J. Comp. Physiol. A 193, 363-370. (doi:10.1007/s00359-006-0192-8).
14. Alghamdi A, Dalton L, Phillis A, Rosato E, Mallon EB. 2008 Immune response impairs learning in freeflying bumble-bees. Biol. Lett. 4, 479-481. (doi:10. 1098/rsbl.2008.0331).
15. Bitterman ME, Menzel R, Fietz A, Schäfer S. 1983 Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107-119. (doi:10.1037/0735-7036.97.2.107).
16. Vergoz V, Roussel E, Sandoz J-C, Giurfa M. 2007 Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS ONE 2, e288. (doi:10.1371/journal.pone. 0000288).
17. Riddell CE, Mallon EB. 2006 Insect psychoneuroimmunology: immune response reduces learning in protein starved bumblebees (Bombus terrestris). Brain Behav. Immun. 20, 135-138. (doi:10.1016/j.bbi.2005.06.008). (Pubitemid 43202078)
18. Alaux C et al. 2010 Interactions between (Apis mellifera). Environ. Microbiol. 12, 774-782. (doi:10. 1111/j.1462-2920.2009.02123.x).
19. Naug D. 2009 Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol. Conserv. 142, 2369-2372. (doi:10.1016/j.biocon. 2009.04.007).