The impacts of parasites on hosts and the role that parasites play in ecosystems must be underlain by the load of parasites in individual hosts. To help explain and predict parasite load across a broad range of species, quantitative theory has been developed based on fundamental relationships between organism size, temperature and metabolic rate. Here, we elaborate on an aspect of that ‘scaling theory for parasitism’, and test a previously unexplored prediction, using new data for total ectoparasite load from 263 wild birds of 42 species. We reveal that, despite the expected substantial variation in parasite load among individual hosts, (i) the theory successfully predicts the distinct increase of ectoparasite load with host body size, indicating the importance of geometric scaling constraints on access to host resources, (ii) ectoparasite load appears ultimately limited by access—not to host space—but to host energy, and (iii) there is a currency-dependent shift in taxonomic dominance of parasite load on larger birds. Hence, these results reveal a seemingly new macroecological pattern, underscore the utility of energy flux as a currency for parasitism and highlight the promise of using scaling theory to provide baseline expectations for parasite load for a diversity of host species.

1. Metabolic costs associated with parasites should not be limited to established infections. Even during initial exposure to questing and attacking parasites, hosts can enact behavioural and physiological responses that could also incur metabolic costs. However, few studies have measured these costs directly. Hence, little is known about metabolic costs arising from parasite exposure. 2. Furthermore, no one has yet measured whether and how previous infection history modulates metabolic responses to parasite exposure. 3. Here, using the California killifish Fundulus parvipinnis and its brain-infecting parasite Euhaplorchis californiensis, we quantified how killifish metabolism, behaviour and osmoregulatory phenotype changed upon acute exposure to parasite infectious stages (i.e. cercariae), and with long-term infection. 4. Exposure to cercariae caused both naïve and long-term infected killifish to acutely increase their metabolic rate and activity, indicating detection and response to parasite infectious stages. Additionally, these metabolic and behavioural effects were moderately stronger in long-term infected hosts than naïve killifish, suggesting that hosts may develop learned behavioural responses, nociceptor sensitization and/or acute immune mechanisms to limit new infections. 5. Although established infection altered the metabolic response to parasite exposure, established infection did not alter standard metabolic rate, routine metabolic rate, maximum metabolic rate, aerobic scope or citrate synthase enzyme activity. 6. Unexpectedly, established infection reduced lactate dehydrogenase enzyme activity in killifish brains and relative Na + /K +-ATPase abundance in gills, suggesting novel mechanisms by which E. californiensis may alter its hosts' behaviour and osmoregulation. 7. Thus, we provide empirical evidence that parasites can disrupt the metabolism of their host both during parasite exposure and after infection is established. This response may be modulated by previous infection history, with probable knock-on effects for host performance, brain energy metabolism, osmoregulation and ecology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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