The Relevance of Time in Biological Scaling

Abstract

Various phenotypic traits relate to the size of a living system in regular but often disproportionate (allometric) ways. These “biological scaling” relationships have been studied by biologists for over a century, but their causes remain hotly debated. Here, I focus on the patterns and possible causes of the body-mass scaling of the rates/durations of various biological processes and life-history events, i.e., the “pace of life”. Many biologists have regarded the rate of metabolism or energy use as the master driver of the “pace of life” and its scaling with body size. Although this “energy perspective” has provided valuable insight, here I argue that a “time perspective” may be equally or even more important. I evaluate various major ways that time may be relevant in biological scaling, including as (1) an independent “fourth dimension” in biological dimensional analyses, (2) a universal “biological clock” that synchronizes various biological rates/durations, (3) a scaling method that uses various biological time periods (allochrony) as scaling metrics, rather than various measures of physical size (allometry), as traditionally performed, (4) an ultimate body-size-related constraint on the rates/timing of biological processes/events that is set by the inevitability of death, and (5) a geological “deep time” approach for viewing the evolution of biological scaling patterns. Although previously proposed universal four-dimensional space-time and “biological clock” views of biological scaling are problematic, novel approaches using allochronic analyses and time perspectives based on size-related rates of individual mortality and species origination/extinction may provide new valuable insights.

Offspring size resolves a latitudinal population growth rate paradox in rays and skates

“…larger in tropical rays and smaller in cool-water skates, and may explain this exception to the TSR where tropical rays attain larger sizes at higher temperatures [64]. Instead, our findings are more consistent with a mortality theory of life histories, and specifically the mortality arising from predation risk and offspring size [10,65].…”

Power and Efficiency in Living Systems

“…Indeed, some biologists have argued that natural selection should generally favor minimal maintenance costs (basal metabolic rates) whenever possible (e.g., [154]). Moreover, among species, two major indicators of fitness-reproductive rate (intrinsic rate of increase) and survival (longevity)-can vary independently of metabolic rate (e.g., [151,[155][156][157]).…”

“…H. Brown and colleagues [14] have also claimed that (re)productive power varies interspecifically as a trade-off with generation time. However, I would suggest that this negative covariation arises because both parameters are related to mortality rate, the ultimate driver of life history variation [157,235], but in opposite ways. As body size increases, mortality rate declines (as is well known: see, e.g., [236][237][238][239]; and references cited in [102,235]), because larger organisms are more protected against predators and other environmental hazards than are more vulnerable, small organisms [101,102,157,235].…”

“…However, I would suggest that this negative covariation arises because both parameters are related to mortality rate, the ultimate driver of life history variation [157,235], but in opposite ways. As body size increases, mortality rate declines (as is well known: see, e.g., [236][237][238][239]; and references cited in [102,235]), because larger organisms are more protected against predators and other environmental hazards than are more vulnerable, small organisms [101,102,157,235]. As a result, smaller organisms have both shorter generation times (they die sooner) and higher reproductive rates to compensate for higher mortality rates than do larger organisms (also see Section 7.7).…”

“…Predation and other environmental hazards tend to cause greater mortality rates in small versus large organisms [101,102,157,235]. As a result, it can be inferred that the population densities of small organisms should more often be below the resource capacity of their environments (i.e., their carrying capacity K), thus enhancing resource availability per individual, as compared to larger, more protected organisms whose populations should more often be near their K, thus causing intense intraspecific competition for limited resources [101,102,157]. This pattern, which has been canonized as a "Serengeti Rule" [314] because of its clear demonstration in mammals of the Serengeti ecosystem [315,316], is likely common across many kinds of taxa and ecosystems [101], but still needs further testing.…”