Limits...
Energy-information trade-offs between movement and sensing.

MacIver MA, Patankar NA, Shirgaonkar AA - PLoS Comput. Biol. (2010)

Bottom Line: 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 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, Northwestern University, Evanston, Illinois, USA.

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.

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Net propulsive force from fin calculated from Eq. 5 across a set of ribbon fin undulation frequencies versus body pitch angle, compared to drag force.In order to be free swimming at constant velocity, the generated thrust must equal drag. Dash-dotted line shows the estimated drag on the body using the equation  where  is the total power needed to overcome measured drag at 15 cm/s and zero pitch angle for the fish cast (0.3 mW), and the velocity of the fish is allowed to vary (see Materials and Methods).
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pcbi-1000769-g006: Net propulsive force from fin calculated from Eq. 5 across a set of ribbon fin undulation frequencies versus body pitch angle, compared to drag force.In order to be free swimming at constant velocity, the generated thrust must equal drag. Dash-dotted line shows the estimated drag on the body using the equation where is the total power needed to overcome measured drag at 15 cm/s and zero pitch angle for the fish cast (0.3 mW), and the velocity of the fish is allowed to vary (see Materials and Methods).

Mentions: Changing the pitch of the body not only affects the drag on the body, and the search rate, it also affects propulsion. The black ghost knifefish generates force by undulating the extended ribbon fin along its underside (Figure 1A) while keeping its body semirigid except for bends to turn left or right [20], [21]. The fin undulations are approximately sinusoidal and travel from one end of the fin to the other—from head to tail for forward movement. The fin generates two different forces: one along the length of the fin (called surge), and one smaller force perpendicular to the fin, pushing the body up (called heave) [21]. As the fin tilts, the forward propulsive force reaches a maximum when the fin base is at an angle of approximately to the horizontal. This is its angle when the body axis is horizontal (e.g., when , then the fin base is at angle in Figure 1B, approximately ). As the fin base tilts past ( body pitch), the sum of the surge and heave forces projected to the forward direction decreases. This effect is shown by Figure 6, which depicts a family of curves relating forward propulsive force to body pitch (Figure 6). For the purposes of this illustration, we assume that the fish varies its frequency of undulation to vary propulsive force. This appears to be true [20].


Energy-information trade-offs between movement and sensing.

MacIver MA, Patankar NA, Shirgaonkar AA - PLoS Comput. Biol. (2010)

Net propulsive force from fin calculated from Eq. 5 across a set of ribbon fin undulation frequencies versus body pitch angle, compared to drag force.In order to be free swimming at constant velocity, the generated thrust must equal drag. Dash-dotted line shows the estimated drag on the body using the equation  where  is the total power needed to overcome measured drag at 15 cm/s and zero pitch angle for the fish cast (0.3 mW), and the velocity of the fish is allowed to vary (see Materials and Methods).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2865506&req=5

pcbi-1000769-g006: Net propulsive force from fin calculated from Eq. 5 across a set of ribbon fin undulation frequencies versus body pitch angle, compared to drag force.In order to be free swimming at constant velocity, the generated thrust must equal drag. Dash-dotted line shows the estimated drag on the body using the equation where is the total power needed to overcome measured drag at 15 cm/s and zero pitch angle for the fish cast (0.3 mW), and the velocity of the fish is allowed to vary (see Materials and Methods).
Mentions: Changing the pitch of the body not only affects the drag on the body, and the search rate, it also affects propulsion. The black ghost knifefish generates force by undulating the extended ribbon fin along its underside (Figure 1A) while keeping its body semirigid except for bends to turn left or right [20], [21]. The fin undulations are approximately sinusoidal and travel from one end of the fin to the other—from head to tail for forward movement. The fin generates two different forces: one along the length of the fin (called surge), and one smaller force perpendicular to the fin, pushing the body up (called heave) [21]. As the fin tilts, the forward propulsive force reaches a maximum when the fin base is at an angle of approximately to the horizontal. This is its angle when the body axis is horizontal (e.g., when , then the fin base is at angle in Figure 1B, approximately ). As the fin base tilts past ( body pitch), the sum of the surge and heave forces projected to the forward direction decreases. This effect is shown by Figure 6, which depicts a family of curves relating forward propulsive force to body pitch (Figure 6). For the purposes of this illustration, we assume that the fish varies its frequency of undulation to vary propulsive force. This appears to be true [20].

Bottom Line: 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 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, Northwestern University, Evanston, Illinois, USA.

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.

Show MeSH