Weather and topography regulate the benefit of a conditionally helpful parasite

Heat‐induced mass mortalities involving ecosystem engineers may have long‐lasting detrimental effects at the community level, eliminating the ecosystem services they provide. Intertidal mussels are ecologically and economically valuable with some populations facing unprecedented heat‐induced mass mortalities. Critically, mussels are also frequently infested by endolithic parasites that modify shell albedo, hence reducing overheating and mortality rates under heat stress. Using a biophysical model, we explored the topographical and meteorological conditions under which endolithically driven thermal buffering becomes critical to survival. Based on meteorological data from a global climate analysis, we modelled body temperatures of infested and non‐infested mussels over the last decade (2010–2020) at nine sites spread across c. 20° of latitude. We show that thermal buffering is enhanced where and when heat stress is greatest, that is, on sun‐exposed surfaces under high solar radiation and high air temperature. These results suggest that new co‐evolutionary pathways are likely to open for these symbiotic organisms as climate continues to change, potentially tipping the balance of the relationship from a parasitic to a more mutualistic one. However, endolithically driven reductions in body temperatures can also occur at or below optimal temperatures, thereby reducing the host's metabolic rates and making the interplay of positive and negative effects complex. In parallel, we hindcasted body temperatures using empirical data from nearby weather stations and found that predictions were very similar with those obtained from two global climate reanalyses (i.e. NCEP‐DOE Reanalysis 2 and ECMWF Reanalysis v5). This result holds great promise for modelling the distribution of terrestrial ectotherms at ecologically relevant spatiotemporal scales, as it suggests we can reasonably bypass the practical issues associated with weather stations. For intertidal ectotherms, however, the challenge will be incorporating body temperatures over the full tidal cycle. 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.