Healy et al. (2013)
Metabolic Rate, Body Size, and Time Perception
Body size and metabolic rate constrain species interactions and their ecological niche.
The resolution of perceived temporal information is often overlooked as a constraint.
Visual systems act as gateways to the dynamic environment.
The ability to process visual information restricts interaction with events.
Smaller size and higher metabolic rates favor perception of temporal change over finer timescales.
Critical Flicker Fusion Frequency (CFF) measures the maximum rate of temporal information processing.
Introduction
All biological systems are shaped by universal constraints like body size and metabolic rate.
Sensory limitations significantly shape species interactions but are often overlooked.
The ability to predict motion is crucial in predator-prey interactions and mate location.
While spatial acuity has been studied, the temporal resolution of dynamic information is less explored.
High temporal resolution is fundamental to an organism’s ecology and behavior.
Temporal resolution relates to the perception of time, especially with fast-moving stimuli.
Evolutionarily, there is a trade-off between high temporal resolution and its energetic costs ().
Ecological and environmental factors, along with intrinsic factors (morphology), shape optimal temporal resolution.
Predators of slow-moving prey need less temporal resolution than those hunting fast prey.
The ability to react to a dynamic environment is a key trait.
Coarse temporal resolution impairs tracking moving targets, as seen in tiger beetles.
Humans face limitations in tracking fast-moving objects in sports.
Body Size, Metabolic Rate, and Temporal Resolution
Body size and metabolic rate affect an individual’s ability to interact with the environment on short timescales.
Larger body sizes reduce maneuverability, while higher metabolic rates increase information processing ability.
The hypothesis is that smaller organisms with higher metabolic rates perceive temporal change on finer timescales.
Neural firing is binary, so temporal resolution is encoded in discrete units.
Visual systems discretize continuous-time and space information and integrate it over time.
Integration time is quantified using Critical Flicker Fusion Frequency (CFF).
CFF is the lowest frequency at which a flickering light is perceived as constant.
Maximum CFF, measured in a response curve of CFF against light intensity, represents the temporal resolution of the sensory system.
The study compares CFF in vertebrates (Mammalia, Reptilia, Aves, Amphibia, Elasmobranchii, Actinopterygii).
Phylogenetic comparative methods test if temporal resolution increases with mass-specific metabolic rate and decreases with body mass, controlling for light levels.
Methods
CFF data was collected from literature using behavioral and electroretinogram (ERG) procedures.
Behavioral studies involve training subjects to respond to changes in light perception.
ERG studies measure the electrical response of the retina to flashing light.
Behavioral studies may measure lower CFF values due to further processing of temporal information.
The experimental procedure was a covariate in the models.
The study noted whether each study was a reliable measure of the maximum possible CFF.
Additional analysis included a term based on this assessment as a categorical covariate.
Mean body masses (g) were taken from literature and databases (FishBase, Animal Diversity Web).
Metabolic rates were measured as mass-specific resting metabolic rate (oxygen consumption).
Values were converted to W/g, using of oxygen consumption for comparison.
For ram-ventilation species, resting metabolic rate was extrapolated to swimming speed = 0 m/s.
Metabolic rate values were corrected to using Q10 values for ectotherms.
Temperature-corrected mass-specific resting metabolic rates (qWg) were used.
Body mass and mass-specific metabolic rate are expected to be correlated according to an exponent of 0.25.
Both terms were included instead of using residuals from a regression of body mass against mass-specific metabolic rate.
There’s a trade-off between sensitivity and movement perception in low light conditions.
Light levels were included as a categorical variable based on species' foraging habits (high or low light).
Turbid water and deep-sea species were categorized as low light environments.
Phylogenetic nonindependence was corrected using a composite tree with divergence times from published molecular phylogenies.
Statistical Analyses
Phylogenetic generalized least-squared approach (PGLS) was used.
PGLS accounts for nonindependence caused by phylogenetic relationships.
The error term consists of a matrix of expected trait covariances calculated using the maximum likelihood estimate of lambda ().
When data structure follows a Brownian motion of trait evolution, . If there is no phylogenetic dependency, .
PGLS models used maximum CFF as the response variable.
Explanatory variables included body mass, qWg, light level (high, low), and experimental procedure (ERG, behavioral).
Brain mass and methodological optimality were included in the sensitivity analysis.
Interactions were not included due to a lack of a priori reasons.
The Akaike information criterion (AIC) was used to select the minimum adequate model.
Results
The most parsimonious model included body mass, log10 of temperature-corrected mass-specific resting metabolic rate (qWg), and light level.
The second most parsimonious model retained all tested variables.
Body mass had a negative effect on the temporal resolution of the sensory system.
A change in body mass of approximately 10 kg resulted in a reduction in CFF of 2 Hz.
Metabolic rate was positively associated with CFF after correcting for mass.
Low environmental light levels were associated with an overall reduction in CFF.
Phylogeny had a minimal effect on the resulting models ().
Experimental type was not correlated with CFF.
Small animals with high mass-specific metabolic rates in high light environments possessed the highest maximum CFF.
Large animals with low mass-specific metabolic rates in low light environments had the lowest CFF.
Results were robust to sensitivity analysis on temperature used to correct ectotherms qWg and the optimality of study methodology for measuring maximum CFF.
Including brain mass did not change the effect of light levels, qWg, and body mass on maximum CFF.
Discussion
Interspecific and intraspecific interactions rely on the ability of organisms to process high temporal resolution sensory information.
Body mass and metabolic rate act as important general constraints on this ability.
This is the first study to indicate a general trend in the ability of vertebrates to resolve temporal information.
Previous studies have focused on specific cases of sensory adaptations.
The findings illustrate the relationship between physiology and the effects of body mass on the ability to resolve temporal features of the environment on fine timescales.
Autrum’s hypothesis predicts that organisms that demand fast visual systems will acquire adaptations increasing CFF values.
One adaptation of altering the physiology and metabolism associated with the visual processing systems is seen in the localized heating of tissues in the heads of blowflies and the eyes of predatory swordfish.
These tissues increase the temperature around the sensory tissues associated with the blowfly’s or swordfish’s visual system, which allows for an upregulation of CFF.
Similar adaptations are also seen across species of large, fast-swimming predatory billfish and Lamnidae sharks.
Physiological adaptations for high-resolution motion detection are also found within specific areas of the retina in some flies, such as the ‘love spot’.
Alterations to the rate of neuron firing, a fundamental limit to the rate of information transfer, through the provision of energy or changes in the physiological environment, would also allow for selection on temporal resolution abilities on a neurological level.
Maneuverability, as defined by the ability to change body position or orientation, generally scales negatively with body mass.
Larger animals physically respond less quickly to a stimulus.
Selection is expected against costly investment in sensory systems with unnecessarily high temporal resolution in large animals, as information on such timescales can no longer be utilized effectively.
Faster and more maneuverable fly species have higher temporal resolutions, and less maneuverable scavenger crabs display slower response dynamics than deeper living predatory species.
The effects of body size and metabolic rate on temporal resolution and the presence of sensory adaptations point towards an interesting dimension of niche space.
Disparity in size and metabolic rate among species within an ecological setting may select for particular sets of adaptations creating a diverse set of sensory systems and interactions.
Species might occupy the same spatial and temporal niche but could be separated due to differential responsiveness to environmental signals and cues.
It seems theoretically possible to encode information in high-frequency signals that can be detected by intended receivers but that are not susceptible to ‘eavesdropping’ by (generally larger) predators.
Ecological systems in which this may be apparent include deep-sea systems where visual signaling is an important determinant of the ability of organisms to interact.
Conclusion
The evolution of sensory systems is subject to limitations imposed by metabolic rate and body mass over orders of magnitude in scale.
Deviations from the expected relationship between temporal perception, body size, and metabolic rate are predicted to be subject to selection pressures for physiological, morphological, and behavioral adaptations that alleviate these constraints.
Temporal resolution may play a much more important role in sensory ecology than previously indicated because of its universal effects relating to body size.
Further investigations into both the underlying mechanisms of these findings and their importance to ecological functioning are needed.