Ontogenetic asymmetry in energetics overturns basic ecological principles

Background/Question/Methods: Ontogenetic development of individuals between their time of birth and maturation characterizes the life history of virtually all biological species and uniquely distinguishes the fundamental units of ecology from those in other fields of natural science. Yet, classic ecological theory about population and community dynamics only accounts for individual reproduction and mortality and often ignores development altogether. If individual life history is accounted for, such as in age-structured matrix models, the relation with population dynamics is mostly unidirectional, i.e. life history influences population dynamics, but not vice versa. Theory about bidirectional influences between individual development and population or community dynamics, referred to as “eco-devo” dynamics, is scarce at best. We consider growth in body size, which is in many species the most prominent aspect of ontogenetic development, and its dependence on the availability of food that is affected by the feedback of population foraging. We analyze whether and how accounting for food-dependent ontogenetic development in population models affects basic ecological principles derived from classic theory that only accounts for individual reproduction and mortality.

Results/Conclusions: We show that size-structured population models accounting for food-dependent growth in body size of individuals can be rigorously simplified to unstructured models only when the mass-specific rate of new biomass production through somatic growth and reproduction is independent of individual body size. This limiting condition of ontogenetic symmetry in energetics separates two broad, more general domains with ontogenetic asymmetry, in which either juveniles or adults have a higher mass-specific net-biomass production. In case of ontogenetic asymmetry we show that basic, well-known ecological principles no longer hold. In particular, for consumer species ontogenetic asymmetry may lead to positive relationships between total population biomass and individual mortality. Predators of such consumers can then increase the abundance of their prey merely by foraging on them. The positive mortality-biomass relation also allows that a doubly handicapped consumer species, which is ousted by its competitor when competing for resources and in addition is preferentially preyed upon by a shared predator, nonetheless is the only consumer species surviving the predation pressure. We thus conclude that basic, unstructured ecological theory only represents the very limiting case of ontogenetic symmetry in energetics and emphasize the need to consider community consequences of the more general condition of ontogenetic asymmetry.