Energetic scaling across different host densities and its consequences for pathogen proliferation

The spread of infectious disease is determined by the ability of a pathogen to proliferate within and spread between susceptible hosts. Processes that limit the performance of a pathogen thus occur at two scales: varying with both the availability of energy within a host, and the number of susceptible hosts in a patch. When the rate at which a host intakes and expends energy is density‐dependent, these two processes are intimately linked. By modifying how hosts compete for and expend resources, a shift in population density may contribute to differences in the flow of energy in a host–pathogen system, both in terms of the energy available for a host to grow, reproduce and fight infection, as well as the energy available for a pathogen to exploit. Energy flux, therefore, connects the two contrasting scales of within‐ and between‐host dynamics by directly linking the proliferation of a pathogen to the number of hosts circulating within a patch. We use the host Daphnia magna to explore the relationship between energy intake and expenditure at various population densities, as estimated by feeding and metabolic rates respectively. By infecting hosts with the bacterial pathogen Pasteuria ramosa, we then explore how infection changes the relative balance of energy intake and expenditure, and how this energy scope translates into production of transmission spores. Our work demonstrates that energy intake declines at a faster rate with density than does metabolic rate, leaving more excess energy (i.e. discretionary energy) available for both hosts and their dependent pathogens at low population densities. This energetic advantage translates positively into host and pathogen growth, with the production of mature transmission spores benefiting most from correlated changes in host body size, as well as a direct connection between energy scope and spore loads. Our findings reinforce how patch quality for a pathogen operates at two contrasting scales, with the within‐host proliferation of a pathogen being optimised in energy rich, low density host populations and opportunities for between‐host transmission likely maximised in dense populations. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.