Foul‐weather friends: Modelling thermal stress mitigation by symbiotic endolithic microbes in a changing environment

Abstract

Temperature extremes are predicted to intensify with climate change. These extremes are rapidly emerging as a powerful driver of species distributional changes with the capacity to disrupt the functioning and provision of services of entire ecosystems, particularly when they challenge ecosystem engineers. The subsequent search for a robust framework to forecast the consequences of these changes mostly ignores within‐species variation in thermal sensitivity. Such variation can be intrinsic, but can also reflect species interactions. Intertidal mussels are important ecosystem engineers that host symbiotic endoliths in their shells. These endoliths unexpectedly act as conditionally beneficial parasites that enhance the host's resistance to intense heat stress. To understand how this relationship may be altered under environmental change, we examined the conditions under which it becomes advantageous by reducing body temperature. We deployed biomimetic sensors (robomussels), built using shells of mussels (Mytilus galloprovincialis) that were or were not infested by endoliths, at nine European locations spanning a temperature gradient across 22°of latitude (Orkney, Scotland to the Algarve, Portugal). Daily wind speed and solar radiation explained the maximum variation in the difference in temperature between infested and non‐infested robomussels; the largest difference occurred under low wind speed and high solar radiation. From the robomussel data, we inferred body temperature differences between infested and non‐infested mussels during known heatwaves that induced mass mortality of the mussel Mytilus edulis along the coast of the English Channel in summer 2018 to quantify the thermal advantage of endolith infestation during temperature extremes. Under these conditions, endoliths provided thermal buffering of between 1.7°C and 4.8°C. Our results strongly suggest that sustainability of intertidal mussel beds will increasingly depend on the thermal buffering provided by endoliths. More generally, this work shows that biomimetic models indicate that within‐species thermal sensitivity to global warming can be modulated by species interactions, using an intertidal host–symbiont relationship as an example.

Weather and topography regulate the benefit of a conditionally helpful parasite

“…Thermal buffering is, however, advantageous when heat stress is greatest, that is, on sun‐exposed surfaces, between midday and late afternoon, during hot weather, with clear skies and light winds. The context‐dependent protection against harmful temperatures can make a difference during heat waves by giving infested mussels a higher chance of survival (Gehman & Harley, 2019; Zardi et al., 2021). This result is particularly relevant for populations of intertidal mussels, which, like most intertidal ectotherms, live at or near the upper limits of their thermal tolerances (Somero, 2010).…”

“…The method uses sudden drops in logger temperatures and the corresponding tidal height at this time to estimate when robomussels are first immersed by the returning tide. We obtained hourly tidal predictions (using the XTide software; https://flaterco.com/xtide/) for nearby maritime ports (Table S2) and interpolated tidal levels at 30‐min intervals (using na.approx function from the r package zoo ; Zeileis & Grothendieck, 2005) to match the time at which robomussels were set to record temperature (see Zardi et al., 2021). We retrieved all tidal levels that were associated with a temperature drop of >8°C in 30 min during incoming tides.…”

“…To validate the approach and select the most suited source of meteorological data, we compared our predictions of Tb non‐infested and Tb infested with temperature data recorded in‐situ using robomussels (Judge et al., 2018) previously deployed at our nine study sites in summer 2017 and 2018 (Figure S2 and Table S1, but see Zardi et al., 2021 for details). At each site, three to six pairs of robomussels (one infested and one non‐infested using shells of Mytilus galloprovincialis ) were deployed within the mid‐mussel zone on a relatively flat surface (<20°) and equidistant from each other ( c .…”

“…In the original study, Zardi et al. (2021) did not measure the exact slope and aspect of the surface where robomussels were placed. Therefore, we chose to infer their topographic orientation by searching for the combination of aspect and inclination angle that best described temperatures recorded in‐situ by robomussels during aerial exposure.…”

“…In these species, endolithic microbes can cause considerable shell damage, reducing scope for growth by increasing metabolic maintenance costs (Ndhlovu et al., 2020), eventually leading to host death through shell collapse (Kaehler & McQuaid, 1999). During extreme warming events, however, this symbiotic association can become advantageous (Gehman & Harley, 2019; Zardi et al., 2016, 2021) as discolouration of the shell caused by endolithic activity enhances solar reflectivity so that infested mussels can be 5°C cooler than non‐infested individuals, potentially increasing host survival rates during heat waves (Gehman & Harley, 2019; Zardi et al., 2016).…”