title: Energy-information trade-offs between movement and sensing.
abstract: While there is accumulating evidence for the importance of the metabolic cost of information in sensory systems, how these costs are traded-off with movement when sensing is closely linked to movement is poorly understood. For example, if an animal needs to search a given amount of space beyond the range of its vision system, is it better to evolve a higher acuity visual system, or evolve a body movement system that can more rapidly move the body over that space? How is this trade-off dependent upon the three-dimensional shape of the field of sensory sensitivity (hereafter, sensorium)? How is it dependent upon sensorium mobility, either through rotation of the sensorium via muscles at the base of the sense organ (e.g., eye or pinna muscles) or neck rotation, or by whole body movement through space? Here we show that in an aquatic model system, the electric fish, a choice to swim in a more inefficient manner during prey search results in a higher prey encounter rate due to better sensory performance. The increase in prey encounter rate more than counterbalances the additional energy expended in swimming inefficiently. The reduction of swimming efficiency for improved sensing arises because positioning the sensory receptor surface to scan more space per unit time results in an increase in the area of the body pushing through the fluid, increasing wasteful body drag forces. We show that the improvement in sensory performance that occurs with the costly repositioning of the body depends upon having an elongated sensorium shape. Finally, we show that if the fish was able to reorient their sensorium independent of body movement, as fish with movable eyes can, there would be significant energy savings. This provides insight into the ubiquity of sensory organ mobility in animal design. This study exposes important links between the morphology of the sensorium, sensorium mobility, and behavioral strategy for maximally extracting energy from the environment. An "infomechanical" approach to complex behavior helps to elucidate how animals distribute functions across sensory systems and movement systems with their diverse energy loads.
authors.affiliation: Department of Mechanical Engineering, Northwestern University, Evanston, Illinois, USA.
authors.forename: Malcolm A
authors.initials: MA
authors.lastname: MacIver
authors.forename: Neelesh A
authors.initials: NA
authors.lastname: Patankar
authors.forename: Anup A
authors.initials: AA
authors.lastname: Shirgaonkar
mesh_terms: D000818:Animals; D001696:Biomechanical Phenomena; D004734:Energy Metabolism / Q000502:physiology*; D023702:Gymnotiformes / Q000502:physiology*; D008124:Locomotion / Q000502:physiology; D008954:Models, Biological; D011235:Predatory Behavior / Q000502:physiology*; D012677:Sensation / Q000502:physiology*; D013550:Swimming
references.citation: J Acoust Soc Am. 1991 May;89(5):2430-4
references.pmid: 1861003
references.citation: J Exp Biol. 2008 Nov;211(Pt 21):3490-503
references.pmid: 18931321
references.citation: Oecologia. 2003 Dec;137(4):502-11
references.pmid: 14505027
references.citation: J Neurosci Methods. 2000 Feb 15;95(2):133-43
references.pmid: 10752484
references.citation: J Comp Physiol A. 1999 Oct;185(4):341-52
references.pmid: 10555268
references.citation: J Exp Biol. 1999 May;202(Pt 10):1195-203
references.pmid: 10210661
references.citation: Nature. 2006 Apr 6;440(7085):757-63
references.pmid: 16598249
references.citation: Integr Comp Biol. 2002 Feb;42(1):127-34
references.pmid: 21708701
references.citation: PLoS Biol. 2007 Nov;5(11):e301
references.pmid: 18001151
references.citation: J Exp Biol. 2001 Feb;204(Pt 3):543-57
references.pmid: 11171305
references.citation: PLoS Biol. 2009 Sep;7(9):e1000203
references.pmid: 19787026
references.citation: Brain Behav Evol. 1992;40(2-3):98-111
references.pmid: 1422810
references.citation: Otolaryngol Head Neck Surg. 1998 Sep;119(3):182-92
references.pmid: 9743074
references.citation: Environ Toxicol Chem. 2005 Sep;24(9):2341-9
references.pmid: 16193764
references.citation: J Exp Biol. 2003 Jan;206(Pt 1):171-80
references.pmid: 12456707
references.citation: Somatosens Mot Res. 2005 Sep;22(3):97-114
references.pmid: 16338819
references.citation: J Exp Biol. 2008 Mar;211(Pt 6):1012-20
references.pmid: 18310126
references.citation: J Exp Biol. 2008 Jun;211(Pt 11):1792-804
references.pmid: 18490395
references.citation: J Acoust Soc Am. 2003 Aug;114(2):1120-31
references.pmid: 12942989
references.citation: J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006 Jun;192(6):573-86
references.pmid: 16645885