# Symbiont-induced phenotypic variation in an ecosystem engineer mediates thermal stress for the associated community

Gerardo Zardi, Laurent Seuront, Christopher Mcquaid, William Froneman, Katy Nicastro

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## ► To cite this version:

Gerardo Zardi, Laurent Seuront, Christopher Mcquaid, William Froneman, Katy Nicastro. Symbiont-induced phenotypic variation in an ecosystem engineer mediates thermal stress for the associated community. Journal of Thermal Biology, 2023, 112, pp.103428. 10.1016/j.jtherbio.2022.103428. hal-04252944

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1 Symbiont-induced phenotypic variation in an ecosystem

2 engineer mediates thermal stress for the associated community

3

4 Gerardo I. Zardi¹,², Laurent Seuront²,³,⁴, Christopher D McQuaid², William Froneman², Katy

5 R. Nicastro²,³,⁵*

6

7

8 ¹Normandie Université, UNICAEN, Laboratoire Biologie des Organismes et Ecosystèmes

9 Aquatiques, UMR8067 BOREA (CNRS, MNHN, UPMC, UCBN, IRD-207), 14000 Caen,

10 France

11 ²Department of Zoology and Entomology, Rhodes University, Grahamstown, 6140 South

12 Africa

13 ³Univ. Lille, CNRS, Univ. Littoral Côte d'Opale, UMR 8187 – LOG – Laboratoire

14 d'Océanologie et de Géosciences, F-59000 Lille, France

15 ⁴Department of Marine Resources and Energy, Tokyo University of Marine Science and

16 Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477 Japan

17 ⁵CCMAR-Centro de Ciencias do Mar, CIMAR Laboratório Associado, Universidade do

18 Algarve, Campus de Gambelas, Faro, 8005-139 Portugal

19

20 *corresponding author: email: katynicastro@gmail.com

21 Declarations of interest: none'

22

23 **Abstract**

24 Microbial symbionts have strong potential to mediate responses to climate change. Such

25 modulation may be particularly important in the case of hosts that modify the physical habitat

26 structure. By transforming the habitats, ecosystem engineers alter resource availability and

27 modulate environmental conditions which, in turn, indirectly shape the community associated

28 with that habitat. Endolithic cyanobacteria are known to reduce the body temperatures of

29 infested mussels and here, we assessed whether the thermal benefits of endoliths on the

30 intertidal reef-building mussel *Mytilus galloprovincialis* extends to the invertebrate community

31 utilising mussel beds as habitat. Artificial reefs of biomimetic mussels either colonised or not

32 colonised by microbial endoliths were used to test whether infauna species (the limpet

33 *Patella vulgata*, the snail *Littorina littorea* and mussel recruits) in a mussel bed with

34 symbionts experience lower body temperatures than those within a bed composed of
mussels without symbionts. We found that infaunal individuals benefitted from being
surrounded by mussels with symbionts, an effect that may be particularly critical during
intense heat stress. Indirect effects of biotic interactions, complicate our understanding of
community and ecosystem responses to climate change, especially in cases involving
ecosystem engineers, and accounting for them will improve our predictions.

Keywords: mussel, *Mytilus*, endoliths, intertidal, parasite, climate change.

41 Introduction

By structurally altering their environment, some organisms can disproportionally induce
strong abiotic changes, and indirectly affect other species. This is the case for bioengineers,
also known as ecosystem engineers, or foundation species (Jones et al., 1996; Jones et al.,
1994) that affect other organisms by significantly modifying physical and chemical processes
occurring in the environment and, in so doing, modifying, maintaining, and creating biogenic
habitats. While autogenic bioengineers (e.g., corals, or trees) modify the environment via
their own physical structures (i.e., their living and dead tissues), allogenic bioengineers (e.g.,
woodpeckers, beavers) alter the environment by transforming living or non-living materials
from one physical state to another, via mechanical or other means (Jones et al., 1996; Jones
et al., 1994).

The ecological role of both types of bioengineer is particularly relevant in
environmentally stressful habitats, such as terrestrial deserts, where they protect other
species from the abiotic forces that would otherwise exclude many (e.g., Ellison, 2019), thus
influencing richness and species composition. In the marine realm, intertidal mussels are
striking examples of bioengineers that shape their environment through habitat modification.
Mussels act as both autogenic and allogenic bioengineers because by building dense three-
dimensional monolayered or multilayered aggregations (mussel beds; Arribas et al., 2014;
Gutiérrez et al., 2003) they create and provide a variety of habitats in intertidal and subtidal
waters that act as refuges and habitat for other organisms. Specifically, mussels create hard
substrata and increase habitat complexity, modifying the humidity, thermal and hydrodynamic regimes experienced by the associated communities (Arribas et al., 2013; Arribas et al., 2014; Nicastro et al., 2020; Nicastro et al., 2012). In addition, they modify the sediment by depositing large amounts of pseudo-faeces and other fine particles (Graf and Rosenberg, 1997; Norkko et al., 2006).

In both terrestrial and aquatic systems, the physical properties of a bioengineer can be significantly changed by microscale biotic interactions which, in turn, can have pronounced consequences for its engineering ability. For example, in terrestrial systems, modifications of several plant root traits such as root biomass, structure and elongation, and root nodulation often respond to soil microorganisms including bacteria, fungi, nematodes, protozoa and mycorrhiza (Centenaro et al., 2018). Such alterations can have considerable knock-on effects in terms of soil stabilization and erosion control, phytoremediation, carbon sequestration and agricultural productivity (Li et al., 2006). In the marine environment, seaweeds can modulate their surrounding chemical environment through their metabolic processes (Hurd et al., 2014). Small-scale biological interactions are also important. For example, seaweed photosynthesis can cause lower oxygen concentration in the boundary layer, offering sessile invertebrates such as tube-forming polychaetes that live on the surface of the fronds a refuge from lower pH seawater (Noisette and Hurd, 2018).

In marine mussels, symbiotic microbial endoliths are an archetypical example of the importance of microscale biotic interactions. By living inside mussels' shells, they lower the hosts' albedo and reduce their exposure to heat stress (Zardi et al., 2016). The effect is due to the white discolouration caused by the excavation activity of endoliths and is critical in the context of climate warming. Over the last century, there has been an increase in the frequency and intensity of marine heatwaves (Frölicher et al., 2018). From 1925 to 2016 alone, this has resulted in a 54% increase in annual marine heatwave days globally (Oliver et al., 2018; Holbrook et al., 2020), with these trends projected to increase under enhanced climate change. These extreme climatic events have been reported to trigger dramatic effects in ecosystem engineers with devastating impacts to the ecosystems they support.
Several studies of rocky shore communities portray a general trend of large scale mass mortality events as a result of heat waves in mytilid mussels such as *Mytilus californianus* (Harley, 2008), *M. galloprovincialis* (Petes et al., 2007), and *M. edulis* (Seuront et al., 2019). Under such extreme thermal conditions, endoliths can provide environmental thermal buffering by reducing their body temperature between 1.7°C and 4.8°C as a result of the increase in solar reflectivity with significant reduced mortality rates in the mussel hosts (Zardi et al., 2021; Zardi et al., 2016).

Here, we explore whether the positive effects of this interaction between the intertidal reef-builder bioengineer *Mytilus galloprovincialis* and its symbiotic microbes extend to the infaunal invertebrate community associated with mussel beds. Specifically, through manipulative experiments conducted outside using natural conditions and artificially constructed mussel beds, we tested the following hypotheses: (i) two grazer species (the limpet *Patella vulgata*, the snail *Littorina littorea*) and mussel recruits surrounded by endolith-infested mussels experience lower body temperatures more than those surrounded by non-infested mussels when aerially exposed to high air temperatures, and (ii) the magnitude of the difference between the two types of beds would differ among the three infaunal species, reflecting inherent differences in their own thermal properties and sizes. Specifically, the expectation was that smaller infaunal species smaller in size (the snail and the mussel recruit) would benefit the most from the cooling effect of endoliths.

## 109 Materials and methods

The effects of mussel bed infestation on infauna species were investigated through a series of manipulative experiments where the temperature of an animal's shell was recorded using an infrared thermal camera (Testo 865) and used as a proxy for the organisms' body temperature (Zardi et al., 2016). The limpet *Patella vulgata* (shell length 2.0 - 2.5 cm), the snail *Littorina littorea* (shell length 1.0 - 1.5 cm) and conspecific recruits (shell length 0.5-
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1.5) of the adult mussel are all naturally found as infaunal species within mussel beds.

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Experiments using these three different infauna species were set up on three separate days in September 2019 (18th, 24th and 25th of September for snails, limpets and recruits respectively) at CCMAR, Faro (Portugal), under clear sky conditions, high sun elevation (12-14 h) and gentle to moderate wind speed (8-18 mph). In addition, the temperature of the beds were recorded throughout the experiment at the same time interval by measuring the shell temperature of three mussels for each bed.

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The experiments were conducted using artificial mussel beds made of either non-infested or infested biomimetic mussels as the primary treatment. Biomimetic mussels were constructed by replacing the tissues of mussels with silicon and used to create artificial mussel beds (Lourenço et al., 2017). The degree of infestation can differ markedly, and, based on previous categorization of endolithic infestation (Zardi et al., 2009), infested beds were made of mussels belonging to the infestation categories C and D (i.e., heavy infestation), while non-infested beds were made up of non-infested mussels (i.e., category A). The artificial beds were circular (ca. 20 cm in diameter; Fig. 1), comprising f mussels (5 ± 0.5 cm in length; n ~ 55-65 mussels per bed) arranged vertically to mimic their position in natural beds and held in place with a semi-rigid, white PVC net (mesh size 1 cm) placed around the beds to keep the mussels in place.

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The target infaunal species were introduced to the beds immediately prior to the experiment, after which time the beds were immersed in water (ca. 18 °C) for 15 min and immediately placed on white boards aerially exposed to ambient sunny conditions for 90 min after emersion (Lourenço et al., 2017; Zardi et al., 2016). Infrared thermal images were captured every 5 minutes. New mussel beds were arranged with new mussels for each trial to avoid pseudo-replication.

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Data on the body temperature of each infauna species were analysed separately using a series of 1-way ANOVAs with bed (infested or non-infested) as a fixed factor and the average body temperature of three individuals of either target species in each bed as the dependent variable (i.e., n = 3).

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The series of ANOVAs were undertaken for each time interval, in addition to time zero to exclude the possibility of a significant differences between treatments already present at the start of the experiment. This allowed us to avoid the need for a repeated measures approach by maintaining independent measurements. Levene's test was used to confirm homogeneity of variances of the residuals and when this assumption was not met, even after transformation, a Kruskal-Wallis test was used instead of the parametric approach.

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## Results

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At time zero, there were no significant differences in temperature between treatments (H=0.42, p= 0.512; H=0.42, p= 0.512 and F1,4=0.237, p=0.652 for the limpets, the recruits and the snails respectively; Fig.2a,b,c; Fig. 1S). Five minutes after the start of the experiment, significant differences in the infauna body temperature were recorded, except for recruits for which the effect of treatment was only significant after 10 minutes.

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This trend was then maintained until the end of the experiment, when, after 90 minutes, infaunal body temperatures were, on average, 5.7°C cooler in a mussel bed with symbionts than in a bed without symbionts (4.5°C, 7.9°C and 4.8°C for limpets, recruits and snails respectively).

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There was, however, no effect of treatment on limpet and snail's body temperature at the 25 minute interval (F₁,₄=0.682, p=0.445 and F₁,₄=7.038, p=0.057 respectively) and for recruits after 15 minutes (F₁,₄=1.446, p=0.295).

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## Discussion

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We found that the body temperature of infauna species was lower in mussel beds affected by microbial endolithic communities, showing that effects of microbial endoliths not only reduce the lower body temperatures of the host mussels, but that this thermally mitigating effect ameliorates abiotic conditions within the mussel bed habitat, and leads to reduced body temperatures of infauna.
The main findings of the current investigation are of fundamental ecological and evolutionary relevance. It adds a crucial component to previous research on the widespread, continuously evolving symbiotic relationship between microbes and their hosts. In corals, endolithic microorganisms form distinct and visible bands in the skeleton that are important because they play key roles in carbon and nitrogen cycles but also weaken the coral reefs' structure by enhancing bioerosion (Pernice et al., 2020). In mussels, microbial endoliths bore into mussel shells, weakening the strength of the shell, and the need for shell repair drains energy resources at the expenses of growth, byssal attachment strength and reproduction (Ndhlovu et al., 2021; Zardi et al., 2009). However, the symbiotic relationship between host and microbial endoliths is currently being reshaped by recent, fast-changing environmental conditions. Recently, endoliths have been suggested among the possible factors contributing to survival of coral species to bleaching as they provide an alternative source of energy during these stressful events (Pernice et al., 2020). Similarly, shell discolouration associated with endolithic cyanobacteria in mussels can lower the hosts' body temperature during intense periods of heat stress, enhancing the probability of survival by up to 50% (Zardi et al., 2021; Zardi et al., 2016). Here, we show how microscale, biotic interactions, such as that of a host and its parasite, can have significant knock-on effects at the community level, well beyond the host survival.

Our findings are also relevant in a purely management and conservation context. While a large body of published literature is now reaffirming the huge economic, scientific, and ecological value of biodiversity (Dirzo et al., 2022), a wide-spread biodiversity crisis has been reported with critical detrimental effects on all ecosystems, including coastal systems (Dirzo et al., 2022; Saunders et al., 2020). As the United Nations' Decade on Biodiversity has recently ended (UN Resolution 65/161), the international focus has now shifted towards restoration efforts (UN Resolution 73/284). Shells alone and the complex biogenic reef structures of the whole mussel beds provide a hard, three-dimensional architectural structure that increases habitat diversity in coastal systems (Creed, 2000). Mussel bed habitats boost species richness and diversity of macrofauna, epifauna and fish as compared
198 to nearby, bare sediments or rocks. As well as being harvested, mussel beds also serve as 199 nursery grounds for other commercially exploited species (e.g., Kristensen et al., 2015; 200 Norling et al., 2015). Given such a crucial ecological role in the system, mussel reefs hold 201 great potential for conservation and management efforts as climate change progresses. In 202 particular, mussel aggregations will play an increasingly fundamental role given the 203 increased likelihood of more frequent, longer lasting and more severe heatwaves (IPCC, 204 2022; IPCC, 2012) because of their capacity to regulate microclimatic conditions at relevant 205 organismal scales (Helmuth et al., 2016; Lathlean et al., 2016a; Lathlean et al., 2016b). 206 Critically, thermoregulation by habitat modifiers is particularly relevant within intertidal 207 habitats where organisms are exposed to dramatic environmental change along strong the 208 terrestrial– marine gradient and live close to their thermal tolerance limits, thus increasingly 209 experiencing mass mortalities and population extinctions driven by rising temperatures 210 (Harley, 2011; Jones et al., 2010; Nicastro et al., 2013; Thyrring and Peck, 2021).

211 Although no direct comparison was made, it is interesting that the beneficial effects of adult 212 infestation were particularly strong in the case of mussel recruits. This may reflect their 213 smaller body size and lower thermal inertia than in the case of snails or limpets. The fact that 214 lower body temperatures were experienced by mussel recruits within mussel aggregations 215 infested by microbial endoliths is likely to have major implications for mussel population 216 dynamics. Although, as filter-feeders, mussels can exert considerable predation pressure 217 on their own recruits (Porri et al., 2008), overall, they have a powerful positive effect on 218 recruit abundance throughout the entire species distributional range, in particular for 219 peripheral populations where environmental conditions are usually harsher and adults are 220 fewer (McGrath et al., 1988; Westerbom et al., 2019). The thermoregulatory role of endoliths 221 is thus likely to further promote the positive effect of adults on recruit survival and thus 222 population resilience following severe declines triggered by stressful events, 223 *Conclusion*

224 No organism exists in isolation. Individual organisms live together in an ecosystem and 225 depend on one another. Sometimes the cascading effects of such dependency are greater
226 in magnitude when they involve ecosystem engineers such as mussels. The implications of
227 the thermal buffering of endoliths on the associated community could also be important from
228 a conservation and management perspective. Symbiont-induced effects on important
229 ecosystem engineers may dictate the resistance and resilience of these biogenic habitats,
230 their engineering effects and also the cascading effects to local intertidal biodiversity. This
231 has implications for management of natural resources under changing climatic conditions.

232

233 Acknowledgments

234 This research was funded by Fundação para a Ciência e a Tecnologia (FCT - MEC,
235 Portugal (grant number: UIDB/04326/2020, EXPL/BIA-BMA/0682/2021), the National
236 Research Foundation of South Africa (grant number: 64801), a Pierre Hubert Curien
237 PESSOA grant, both the European Maritime and Fisheries Fund (FEAMP) and France
238 Filière Pêche through the research project SOLACE. This work is a contribution to the CPER
239 research project CLIMIBIO. The authors thank the French Ministère de l'Enseignement
240 Supérieur et de la Recherche, the Hauts de France Region and the European Funds for
241 Regional Economical Development for their financial support to this project.

242

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351 **Figure Legend**

352 **Fig. 1.** Example of an artificial mussel beds (A,B) with associated infauna (the *snail Littorina littorea*) and the corresponding infrared images (C).

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355 **Fig. 2.** Body temperatures (averages and + 95%CI) for the limpet *Patella vulgate*, the recruit of *Mytilus galloprovincialis* and the snail *Littorina littorea* at time zero (A), after 45 minutes (B); and at the end of the experiment (i.e. 90 minutes) (C).

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<figure><img src="image_5.png" /><figcaption>B.</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>C.</figcaption></figure>

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