Symbiotic endolithic microbes alter host morphology and reduce host vulnerability to high environmental temperatures

Abstract

Thermal stresses, such as those associated with global warming, have the potential to change the strength and even the direction of interspecific interactions. On rocky shores, bio‐eroding microbial endoliths infect the mussel Mytilus californianus. Infestation by microbial endoliths can weaken the shell and lead to mechanical failure and death, increased vulnerability to predation, mechanical damage, etc. However, endolith infestation is associated with the loss of the dark‐colored periostracum, exposing the underlying light gray prismatic layer of the shell and potentially reducing stressful heat gain during low tide. We explore the consequences of the mussel–endolith relationship on mussel tolerance to high environmental temperature through a series of experimental manipulations and comparative observations. Experimental sterilization of the shell surface reduces the rate of periostracum loss, suggesting that the change in shell surface color is indeed caused by microbes residing on/in the shell. Eroded shells absorbed less solar energy than shells with their periostracum intact, and mussel mimics with infested shells remained cooler on sunny days. Manipulation of shell color in the field resulted in higher mortality in black‐painted mussels relative to gray‐painted or naturally eroded mussels. Furthermore, following exceedingly hot weather, mortality was significantly lower for heavily infested, light‐colored mussels than for lightly infested, dark‐colored mussels. Thus, although shell‐boring microbes have the potential to act as parasites under the majority of conditions experienced by mussels, they may be critical mutualists during periods of intense thermal stress. This context‐dependent symbiosis may allow mussels to occupy higher shore levels than would otherwise be possible, and thus indirectly benefit the hundreds of species which use mussel beds as habitat.

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

“…Interestingly, a close examination to over 1200 randomly shells collected following this mass mortality event show that the vast majority of them (96 to 100%) had no sign of infestation (Seuront, unpublished data, see Figure S4). Although such observations cannot quantify or confirm the protective roles of endoliths, they complement previous field manipulative experiments in different regions showing that, during heat waves, the moderation of solar heating by endoliths results in significantly lower mortality rates (Gehman & Harley, 2019; Zardi et al, 2016). Interestingly, large‐scale sampling covering a wide latitudinal range (c. 28–37°N) along the coasts of Portugal and Morocco revealed a strong gradient of increasing endolithic infestation of M. galloprovincialis towards lower latitudes, presumably due to the enhancement of endolith photosynthetic activity through greater light availability and decreased cloud cover towards the equator (Lourenço et al, 2017).…”

“…This pronounced phenotypic change provides mussels with a higher degree of thermal buffering that is most likely unreachable through adaptive mutation. It has been suggested that endolithic thermal buffering might be indicative of a transition towards mutualism in the endolith–mussel relationship (Gehman & Harley, 2019; Zardi et al, 2016). Indeed, most mutualisms have evolved from wholly parasitic associations and conditionally beneficial parasites are intermediate stages in a transient relationship triggered by changes in the biotic/abiotic environment (Fellous & Salvaudon, 2009).…”

“…Importantly, recent results have shown that shell corrosion caused by endoliths mitigates the thermal stress experienced by their mussel hosts; mussels with corroded shells experience significantly lower body temperatures leading to significant increases in survival (up to 50%) during heatwaves compared to conspecifics that are not affected by endoliths (Zardi et al, 2016). Such conditional help (sensu Fellous & Salvaudon, 2009) is triggered by reduced absorption of solar energy by mussel shells that are whitened by endolithic boring (Gehman & Harley, 2019; Zardi et al, 2016).…”

Ectoparasites reduce scope for growth in a rocky-shore mussel (Perna perna) by raising maintenance costs

“…Our estimates of lethal temperatures, however, did not differ between clean and infested mussels, suggesting no differences in their physiological sensitivities to future warming or their capacity to activate a heat-shock response to combat the effect of increasing temperatures (Buckley et al, 2001;Hochachka and Somero, 2002;Schneider, 2014;Somero, 2002). Interestingly, because endolithic cyanobacteria increase the reflectivity of solar radiation by the shell, thus reducing body temperature during low-tide when temperatures are stressful, these parasites can even provide a service to their hosts (Gehman and Harley, 2019;Zardi et al, 2016). Together, these earlier biophysical studies and our assessment of the impact of endolithic cyanobacteria on mussel thermal tolerance suggest a net positive effect in the face of short-term thermal stress.…”

Climate Change and Shell-Boring Polychaetes (Annelida: Spionidae): Current State of Knowledge and the Need for More Experimental Research

“…Other case studies have shown that hosts themselves may derive different levels of benefits from these types of symbiotic shifts. For example, studies on endolithic cyanobacteria, which are known to erode the shells of their molluscan hosts, have shown that under climate change stressors, specifically, elevated temperatures, there appears to be a reversal from a parasitic relationship to one that confers benefits to the host (Zardi et al, 2016;Gehman and Harley, 2019). After the dark-colored periostracum is degraded due to the 000 boring activity of the endolith, the lighter-colored prismatic layer reflects rather than absorbs heat; and under experimentally induced thermal stress, infected shellfish exhibit higher survival rates than their uninfected congeners.…”