# Influence of parasitism on bioturbation: from host to ecosystem functioning

Annabelle Dairain, Alexia Legeay, Xavier de Montaudouin

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Annabelle Dairain, Alexia Legeay, Xavier de Montaudouin. Influence of parasitism on bioturbation: from host to ecosystem functioning. Marine Ecology Progress Series, 2019, 619, pp.201-214. 10.3354/meps12967. hal-04216673

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Submitted on 28 Sep 2023

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1 **Influence of parasitism on bioturbation: from host to ecosystem functioning**

3 Annabelle DAIRAIN*, Alexia LEGEAY and Xavier de MONTAUDOUIN

4 Univ. Bordeaux, EPOC, UMR CNRS 5805, F-33400 Talence, France

5 * Corresponding author: annabelle.dairain@u-bordeaux.fr

6 Postal address:

7 UMR 5805 EPOC, Université de Bordeaux, CNRS

8 F-33120 Arcachon, France

9 **Running page head**: Parasitism in bioturbation studies

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11 Abstract

Bioturbating species represent a typical example of ecosystem engineer species in marine benthic environments. These
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abundant endo- or epibenthic organisms modify the physical structure and geochemical properties of sediments, and at
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broader ecosystem scale impact nutrient flows and benthic community structure. The ecological importance of
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bioturbators depends on (1) their abundance and (2) the magnitude of their bioturbation activity. We suggest that parasitism has
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a substantial impact on bioturbators, and cascading effects on their role in ecosystem functioning. Reviewing 5940 papers
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concerning bioturbation and using a set of selective criteria, we identified 176 bioturbating species, with 31 % of
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these potentially parasitized (micro- and macroparasites). However, there is significant discrepancy in the research effort on
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parasites among bioturbating groups, the highest effort being devoted to molluscs whereas studies on annelids and
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arthropods are rare. Furthermore, studies addressing the impacts of parasites on their bioturbating hosts are still scarce, but
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evidence we do have indicates that parasites impair their hosts' physiological state, fecundity, behaviour and survival.
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Because of impacts of parasites on phenotypic traits related to the bioturbation engineering activity of their hosts, parasitism
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could play a key role on ecosystem functioning through cascade effects. Yet, studies assessing the intricate link between
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parasites and their hosts' bioturbation activity, including potential effects on ecosystem functioning, are virtually non-existent.
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25 **Keys words:** bioturbation, parasitism, ecosystem functioning, behaviour modifications, cascade effects

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# 1. INTRODUCTION

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The structure and dynamics of ecosystems are shaped by myriad ecological and environmental factors, an important one of which is the activity of organisms. In 1994, Jones et al. defined ecosystem engineer species (EES) as species that modify their physical environment by their activity (allogenic engineers) or by their mere presence (autogenic engineers) in addition to their potential contribution to biotic interactions.

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The influence of bioturbators as EES on ecosystems depends on (1) their abundance and

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(2) the magnitude of their activities and thus on the physiological state of these organisms. In natural environments, organisms are seldom in optimal environmental conditions and different abiotic and biotic factors can adversely affect the physiology and the behaviour of bioturbating organisms, altering ecosystem functioning through cascade effects. The role of environmental factors such as temperature, salinity, food and oxygen availability is well established (e.g., Berkenbusch & Rowden 1999; Ouellette et al. 2004; Maire et al. 2007; Przeslawski et al. 2009). Biotic interactions can also have a large influence on the individual behaviour of organisms and can play a key role in bioturbation processes (e.g., Braeckman et al. 2010; Maire et al. 2010; Premo & Tyler 2013; Campbell & Lindsay 2014).

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Among biotic factors influencing faunal EES, one major concern is the role played by parasites and associated infectious diseases. In the context of global climate change, it has been suggested that warmer conditions could increase the frequency and intensity of disease events (Harvell et al. 2002; Marcogliese 2001). For example, increase in seawater temperature enhances infection success of the trematode *Maritrema novaezealandense* in the amphipod host *Paracalliope novizealandiae*. A larger parasite burden is associated with a higher mortality rate of amphipods (Studer & Poulin 2013). Although many parasites and associated infectious diseases can produce mass mortality events in host populations (e.g., Jensen & Mouritsen 1992; Jonsson & André 1992; Fredensborg et al. 2004), parasites can also have a wide range of sub-lethal effects, especially on the physiological status and behaviour of infected organisms. For example, the health of parasitized organisms is often impaired as reflected in reduced growth rate and condition index (e.g., Thieltges 2006; Dang et al. 2013; O'Connell-Milne et al. 2016). This pattern could be due to parasites directly interfering with food uptake (Flye-Sainte-Marie et al.

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2007; Stier et al. 2015) or impairing a host's metabolism (Anderson 1977; Repetto & Griffen 2012). Behaviour modifications can also result from parasitism, with infected organisms exhibiting aberrant behaviour compared to unparasitized individuals (e.g., Thomas & Poulin 1998; Pascal 2017). If parasites are prevalent in the population of their host, their effects on individual organisms can produce broad impacts at the ecosystem level, with parasites playing a key role in structuring communities of free-living organisms (Minchella & Scott 1991; Mouritsen & Poulin 2002; Poulin 1999; Price et al. 1986).

The role of parasites on EES acting by bioturbation appears as a crucial issue in the understanding of marine ecosystems. The aim of this paper is to review current knowledge on parasites and associated infectious diseases in common bioturbators, to highlight some scientific gaps and propose a general framework for future studies. We examined the relationship between parasites and bioturbators by answering four questions: (1) what are the commonly studied bioturbating species, (2) are there any parasites known to infect these bioturbating species, (3) what are the effects of parasites on their host, and (4) do parasites infecting bioturbating species have any consequence on the functioning of ecosystems?

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## 2. DEFINITIONS

### 2.1. Type of bioturbators

In this study, bioturbating species were restricted to epi- or endobenthic faunal organisms influencing the physical structure (i.e. grain size, porosity, organic matter content, etc.) and/or biogeochemical properties (i.e. nutrient and solute contents, redox status, etc.) of sediments. In addition, this literature review was limited to invertebrates occurring in coastal environments, including mangrove forests. Taking these restrictions into account, publications were searched in Scopus using the terms "bioturbation", "sediment reworking" and "bioirrigation". Because of the very high number of related papers, the search was further constrained to publications belonging to the "environmental science" subject area for the items "sediment reworking" and "bioirrigation". A list of 4912, 732 and 296 publications for the terms "bioturbation", "sediment reworking" and "bioirrigation" were gathered (May 11th, 2018), respectively. Bioturbators were taxonomically classified based on the World Register of Marine Species (WoRMS Editorial Board 2018). Our search found a total of 176 bioturbating species studied in coastal environments worldwide (Fig. 1; see ESM 1 for a full list of the bioturbators). Species belonging to the phyla Arthropoda, Annelida and Mollusca were the most extensively studied, representing 37, 27 and 23 % of the total number of bioturbator species richness, respectively (Fig. 1).

### 2.2. Type of parasites

Parasites were broadly defined as organisms exploiting other organisms (the hosts) and can include viruses (Combes 1995). This study investigated both microparasites (viruses and unicellular organisms) and macroparasites (mainly helminths and arthropods) of bioturbating species (Anderson & May 1979). For each of the bioturbating species identified in our first search, a second search for publications mentioning parasites occurring in these organisms was made by using the name of the bioturbating species in combination with the terms "parasite",
"infection", "bacteria" and "virus". In addition, we collected data related to prevalence, intensity and/or abundance of parasitic infections when available. In a sampled population, prevalence is defined as the percentage of infected individuals, intensity of infection as the mean number of parasites per parasitized hosts, and abundance as the mean number of parasites per potential host (including both parasite-infected and uninfected) (Margolis et al. 1982). Furthermore, the influence of parasites on the physiological state, behaviour and bioturbating activity of their host was also recorded.

## 3. PARASITE SPECIES INFECTING BIOTURBATING ORGANISMS

Of the 176 species of bioturbators identified, 55 species (i.e. 31%) were reputed as being parasitized with at least one macro- or microparasite species (Fig. 1). More specifically, 27 (i.e. 15%) and 11 (i.e. 6%) bioturbating species are infected with at least one macro- or microparasite species only, respectively and 17 bioturbators (i.e 10%) with both macro- and microparasites (Fig. 1; see ESMs 2 and 3, respectively, for a full list of macro- and microparasites of bioturbating species). There is an important disparity regarding the distribution of parasites across the phyla of bioturbators, with highly parasitized, such as molluscs (51% of the species harbouring at least one parasite species), and others apparently less parasitized, for example echinoderms (22%) and arthropods (23%) (Fig. 1). Similarly, the number of parasite species identified per bioturbating host strongly differed among phyla (Fig. 2). Numerous studies were devoted to bioturbating molluscs and highlighted that they were diversely parasitized, with on average (± SE) 8.2 ± 2.9 macroparasite species (Fig. 2A) and 8.6 ± 2.8 microparasite species (Fig. 2B) identified per individual species. To the contrary, only a few parasites species have been documented in annelids, with on average 1.4 ± 0.3 macroparasite species (Fig. 2A) and 1.8 ± 0.4 microparasite species (Fig. 2B) identified per annelid species. Finally, there was also a large

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variability in parasite species richness per bioturbating species within a given phylum (Fig. 2).

For example, the number of macro- and microparasites identified in molluscan bioturbators ranged from 1–55 and 1–26, respectively (ESMs 2 and 3).

Several factors explain the discrepancy in parasite species richness recorded among and within the phyla of bioturbators. First, through a large meta-analysis, Kamiya et al. (2014) highlighted a positive association between parasite species richness and host body size, population density and geographical range. Second, difference in sensitivity and susceptibility of bioturbating species to parasites could also explain interspecific variation in parasite species richness (Dang et al. 2009). On the other hand, we suggest that the large disparity in parasite species richness we observed among and within phyla of bioturbators is more likely related to a bias in research effort on parasites occurring in these organisms. Notably, the higher the economic value of a species, the more intensive are the research efforts to identify any potential pathogens or other stressors that could influence the sustainability of the production and/or the quality of the resource. For instance, numerous studies have been conducted in molluscs, a phylum of broad interest for fisheries and aquaculture, with the common cockle *C. edule* and the Manila clam *R. phillipinarum* being two important species. Although a small proportion of echinoderms have been described as being parasitized so far, there is a proportionally extensive literature on parasites infecting bioturbating species with a commercial value, such as the sea cucumber *Apostichopus (Stichopus) japonicus*. Accordingly, annelids are poorly exploited and have rarely been studied with regard to parasites and associated infectious diseases.

Bioturbators harbour a large diversity of macro- and microparasites species with large differences in the relative frequency among parasite phyla (Fig. 3, ESMs 2 and 3). Platyhelminthes are the most common macroparasites infecting bioturbators, with 75 % of the
reported parasites species belonging to this phylum. Platyhelminthes infect molluscs,
echinoderms and annelids, and to a lesser extent arthropods (Fig. 3A). Platyhelminthes includes
about 30,000 species (Caira & Littlewood 2013), of which many are parasites (Dobson et al.
2008), such as members of the Trematoda or Cestoda. Moreover, it is one of the most important
groups of marine parasites (Rohde 2005) which makes it unsurprising that infections with
Platyhelminthes have been noted in bioturbators to such extent. On the other hand, only a few
studies highlighted the occurrence of parasitic annelids or nemerteans in bioturbators. As these
two groups mainly consist of free-living organisms, they represent minor parasite group in
marine environments (Rohde 2005). Regarding microparasites, 53 % of the species identified are
eukaryotes and 36 % are bacteria. Eukaryotic microparasites encompass a large diversity of
phyla, while bacteria are mainly represented by Proteobacteria (Fig. 3B). Finally, a few viral
syndromes and infectious diseases for which the etiological agent has not yet been fully
characterized (e.g. various neoplasias, viscera ejection syndrome, brown muscle disease; ESM 3)
have been noted in bioturbating organisms as well.

4. DIRECT EFFECTS OF PARASITES ON BIOTURBATING SPECIES

Parasites have direct effects on their host, i.e. pathological impacts on individuals. The
literature is limited concerning bioturbating species. Our literature survey documented that 376
macroparasites (N = 108 studies) and 188 microparasites and associated infectious diseases (N =
132 studies) parasitize 55 coastal bioturbating species. Among these parasites, impacts on the
host were recognized in 32 % and 36 % of the studies highlighting the occurrence of macro- and
microparasites (and associated infectious diseases) in bioturbating species, respectively. These
direct effects included alterations of physiological state (i.e. modulation of gene expression and
cellular functions, initiation of inflammatory responses, tissue damages, etc.), modifications of
reproductive functions (i.e. partial or total castration, changes in reproductive success, etc.),

increase of the mortality rate of the host and modifications of host behaviour (reduced activity

levels, abnormal behaviours, etc.) (Fig. 4, ESL 2 and 3). More than 82 % of the known impacts of

macroparasites are due to Platyhelminthes (ESM 2). Most studies on microparasites focused on

Proteobacteria (36 %) and Myzozoa (30 %) (ESM 3). These patterns are in accordance with those

showing that Platyhelminthes, Proteobacteria and Myzozoa are the most commonly described

macro- and microparasites in bioturbating species (Fig. 3).

## 4.1. Impacts of parasites on bioturbator physiology

Numerous parasites are documented to impact the physiological state of their bioturbating
host (Fig. 4). At the molecular scale, parasites interfere with gene regulation, thereby either up- or
down-regulating their expression. For example, the trematode *Himasthla elongata* up-regulates
the expression of several genes related to mitochondrial metabolism and oxidative responses in
infected cockles *C. edule*, a reputed bioturbator. These modulations in gene expression are
considered to be a molecular response to parasites causing energetic losses and oxidative stress in
cockles (Paul-Pont et al. 2010). Parasites can also impair the host's physical integrity if
physiological alterations are concomitant with physical injuries. While developing and residing
inside their host, parasites cause significant histopathological damages to host tissue (Lauckner
1980, Robaldo et al. 1999, Dang et al. 2008). For instance, the protozoan parasites *Perkinsus* spp.
induce histological lesions in gills, digestive gland and gonad gland of the sand gaper clam *Mya arenaria* (McLaughlin & Faisal 1998). As the gills and the digestive gland play a key role in
nutrients absorption, such tissue alterations are expected to be energetically costly for the host,
and may have direct repercussions on its growth. In fact, a caging experiment conducted at two
sites impacted by perkinsosis along the northeast Atlantic coast of France demonstrated that
growth rates of the bioturbators *R. decussatus* and *R. philippinarum* are significantly compromised as a result of *Perkinsus* spp. infections (Dang et al. 2013). Macroparasites impacting the growth of their bioturbating host have also been broadly documented (e.g., Mouritsen & Jensen 1994; Pascal et al. 2016; Smith et al. 2008). The mud shrimp *Upogebia* cf. *pusilla* displays reduced size when infected with the epicaridean isopod *Gyge branchialis* (Pascal et al. 2016). The negative effect of the parasite is probably not related to histological lesions but to the parasite directly feeding at the expense of its host (Tucker 1930). By doing so, the parasite strongly affects host energetics (Hughes 1940) and consequently its physiological state (Williams & Boyko 2012). Parasites do not always diminish their host's growth rate. The bioturbators *Peringia* (*Hydrobia* ) *ulvae* infected with trematodes grow to larger sizes than their unparasitized conspecifics (Mouritsen & Jensen 1994). Such cases of gigantism have been reported in several host-parasite association involving parasitic castrators (de Montaudouin et al. 2003; Pearre 1976; Sluiters et al. 1980).

**4.2. Impacts of parasites on bioturbator reproduction**

Evidence for alterations to host fecundity are common and has been found in 31 % and 6 % of the studies on effects of macro- and microparasites, respectively (Fig. 4). Macroparasites, and especially digenean trematodes (Platyhelminthes), are often associated with impairment of the host reproductive function (ESM 2). Digenean trematodes have complex life cycles. One of the stages, called sporocyst or rediae according to digenean species, is fundamentally damaging for the fecundity of the host (Lauckner 1980, 1983). Digenean trematodes infect the digestive gland and/or the gonad of their host (Probst & Kube 1999), causing partial or complete castration via mechanical or chemical damages to host reproductive tissue (Hurd 1990). For instance, infection with trematodes leads to an important reduction of the penis size of the mud snail *P*.
230 *ulvae* and to almost non-existent oviposition in females (Mouritsen & Jensen 1994). Castration is
231 not only caused by digenean trematodes; crustacean parasites like epicaridean isopods have also
232 strong influences on the fecundity of their bioturbator hosts (Dumbauld et al. 2011; Tucker
233 1930). However, castration of hosts by isopods seems to be related to the parasite lowering the
234 condition index of the host and/or interfering with the secretion of host reproductive hormones
235 (Reinhard 1956; Williams & Boyko 2012). In sharp contrast, some parasites such as
236 microsporidian can enhance the fecundity of their bioturbating host (Mautner et al. 2007), but
237 these example are more rare.
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4.3. Impacts of parasites on host mortality

239 As a result of their pathological effects, parasites can compromise the survival of their
240 bioturbating hosts. An increase in mortality rate has been noticed in 17 % and 49 % of the studies
241 evaluating the influence of macro- and microparasites, respectively (Fig. 4). For instance, the
242 Galician population of the common cockle *C. edule* showed an important decline in spring 2012,
243 with mortality up to 100 %. At this time, juvenile and adult cockles were heavily infected (up to
244 100 % prevalence) with the protistan parasite *Marteilia cochillia*, which is probably the cause of
245 the population collapse (Villalba et al. 2014). Marteiliosis is associated with substantial
246 physiological alterations in infected organisms. The parasite infects the digestive gland of its host
247 and interferes with its energetic balance (Pérez Camacho et al. 1997), weakens organisms and
248 eventually kill them.
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249 Among macroparasites, digenean trematodes have been recognized to deeply affect the
250 survival of their hosts, at time causing collapses of natural populations. For instance, the
251 trematodes *Microphallus claviformis* and *Maritrema subdolum* are considered to be the main
252 cause of the 40 % population decline of the bioturbating mud snail *P. ulvae* observed in the
Danish Wadden Sea during Spring 1990 (Jensen & Mouritsen 1992). Digenean trematodes can also modulate the population size structure of their bioturbating hosts because of differential susceptibility to parasitism of small and large organisms. An extensive field survey conducted in Arcachon Bay, France, over the years 1998–1999 indicated an important decline of the largest mud snails *P. ulvae* during the winter 1998-1999 which were also the most parasitized (up to 100 %). A laboratory experiment conducted in parallel highlighted higher mortality rates of parasitized organisms as compared to unparasitized individuals. Together, these results demonstrate that digenean parasites substantially influence the population size structure of the bioturbator *P. ulvae* (de Montaudouin et al. 2003).

**4.4. Impacts of parasites on bioturbator behaviour**

Parasites can have more subtle effects on their hosts such as behaviour alteration. Such effects have been reported in 46 % and 11 % of the studies evaluating the influence of macro- and microparasites on their bioturbating hosts, respectively (Fig. 4; ESMs 2 and 3).

Modifications of the behaviour of the host can be a side effect of parasitism, that is phenotypic alterations with no adaptive value for either the parasite or the host (Ewald 1980). Few examples report how parasites impair the behaviour of bioturbators and their activities (Fig. 4; ESM 2 and 3). For instance, mud snails *P. ulvae* infected with trematode parasites experience modifications of locomotory behaviour, with parasitized snails moving slower and crawling over shorter distances as compared to uninfected organisms (Mouritsen & Jensen 1994). This behavioural modification could be a side effect of parasites interfering with the host energy allocation. Indeed, mud snails exhibited increased growth rates (“gigantism”). Since locomotory activity is a highly costly behaviour, it has been suggested that parasites stimulating host growth reduce the energy available for the host to crawl (Mouritsen & Jensen 1994).
Regarding the impacts of microparasites on host behaviour, the literature is even more scarce, with altered behaviour recognized in only 11 % of the studies documenting the occurrence of microparasites or infectious diseases in bioturbators (Fig. 4; ESM 3). Given the large influence of microparasites on the physiological status of their hosts (ESM 3) it is likely that microparasites have side effects on host behaviour as well. For instance, brown muscle disease causes a serious atrophy of the posterior adductor muscle of the Manila clam *R. philippinarum* (Dang et al. 2008). Any alterations to this muscle is expected to disturb clam feeding and respiration, as well as locomotion. Such modifications of locomotory activity were observed in Manila clams infected with the protozoan *Perkinus olseni*. This parasite promotes the emergence of *R. philippinaum* at the sediment surface and limits its ability to re-burrow in thermally stressful condition (Nam et al. 2018).

Modifications of the behaviour of the host can also be adaptive manipulation. This typically involves parasites with complex life cycles as host behaviour modifications are expected to enhance the transmission success of parasites (Combes 1991; Lafferty 1999; Moore 2002). One of the most detailed examples of adaptive manipulation in bioturbators involves the New Zealand cockle *Austrovenus stutchburyi*, which is commonly found at the sediment surface of tidal flats, with organisms showing difficulty in burrowing (Thomas & Poulin 1998). Surfacing cockles (i.e., in abnormal position) are heavily infected with the trematode *Curtuteria australis*, compared to buried cockles (i.e., in normal position) (Thomas & Poulin 1998). The trematode needs the cockle to be eaten by marine birds to complete its life cycle, which is facilitated by its altered behaviour at the surface of the sediment. Together, these results suggest that the parasite alters the cockle phenotype so as to enhance its own transmission success (Thomas & Poulin 1998).
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# 5. INFLUENCE OF PARASITES ON BIOTURBATION ACTIVITY AND ECOSYSTEM FUNCTIONING

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The direct effects exerted by parasites on individuals can have knock-on effect on the population of bioturbators, then influencing their role as EES. These indirect effects of parasites on ecosystem functioning can be classified as density- and trait-mediated effects (Mouritsen & Poulin 2002; Preston et al. 2016). First, parasites can modify traits of their hosts involved in their functional role within ecosystem. These trait-mediated effects occur as side effect of pathology or are adaptive parasite manipulation. Secondly, through their impacts on the mortality and fecundity of their host, parasites can be main drivers of host density and regulate population size structure.

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## 5.1. Trait-mediated effects

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Out the 215 studies evidencing the occurrence of 376 macro- and 188 microparasites in 55 bioturbating species over 176 bioturbators commonly studied in coastal environments, 82 studies showed that parasites can impair the physiological state, reproductive capacity, behaviour and/or the mortality of their bioturbating hosts. Of these studies, only 21 studies depicted effects of parasites on the behaviour of their bioturbating host. Within these 21 studies just seven focused on the link between the occurrence of parasites and their role in modulating the bioturbating activity of their hosts, with potential outputs on the community of free-living organisms and ecosystem functioning, the so-called trait-mediated effects (Table 1). Nevertheless, these few papers strongly support the idea that parasites can act as EES themselves by modifying functional traits of their host involved in bioturbation activities (Thomas et al. 1999) (Table 1, Fig. 5). For instance, Pascal (2017) monitored the influence of the epicaridean parasite *G. branchialis* on the behaviour of the mud shrimp *U. cf. pusilla* through video recording. He defined four main behavioural states for the mud shrimp species as “resting”,
"burrowing", "ventilating" and "walking". "Burrowing" and "ventilating" are the two behaviours associated with bioturbation activities of the mud shrimp. Pascal (2017) demonstrated that parasitized mud shrimp spend 1.8- and 2.3-fold less "burrowing" and "ventilating" than healthy organisms. These behavioural modifications are associated with negative impacts on the intensity of the bioturbating activity: the sediment reworking rate of parasitized organisms is 4.6-fold lower and the bioirrigation rate 2.9-fold lower compared to unparasitized organisms. As a result, biogeochemical fluxes are also strongly modified. The total oxygen and nitrate uptake are reduced and there is a diminished release of ammonium at the sediment-water interface. This suggests, therefore, that parasitized mud shrimp have a much lower influence on organic matter mineralization and nutrient turnover than uninfected organisms (Pascal 2017). At the ecosystem level, these findings can be highly relevant (Fig. 5) as (1) mud shrimp can attain high densities (e.g., Nates & Felder 1998) and (2) epicarideans are widespread in natural populations of mud shrimp (Pascal et al. 2016; Smith et al. 2008).

Mouritsen & Poulin (2005, 2010) addressed the influence of parasitism on animal community structure (Table 1). Over a long-term field experiment, they highlighted a positive relationship between macrozoobenthic species richness (and density) and the presence of parasitized cockles *A. stutchburyi* (Mouritsen & Poulin 2005). A similar pattern was reported at a larger spatial scale (Mouritsen & Poulin 2010). The bivalve *A. stutchburyi* harbours multiple parasites, some of which can manipulate the behaviour of cockles to facilitate transmission. These behaviour modifications can also change the role of cockles as EES. Heavily parasitized organisms are more likely found at the sediment surface than buried in the sediment and show reduced ability to rebury in the sediment (Thomas & Poulin 1998). Moreover, heavily parasitized cockles exhibit reduced crawling activity compared to moderately infected conspecifics
(Mouritsen & Poulin 2005). Cockles exhibit important reworking activity in subsurface sediments, where they also strongly impact nutrients cycling and the production of primary producers (Sandwell et al. 2009). Mouritsen & Poulin (2005, 2010) suggested that the positive association between macrozoobenthic species richness and parasitized cockles could be related to (1) a lower disturbance of the sediment *via* parasites reducing bioturbating activities of cockles and (2) surfacing cockles acting as physical ecosystem engineers (Jones et al. 1997; Thomas et al. 1998).

There is no general rule regarding the influence of bioturbators on macrofaunal communities. Inhibitory and facilitative effects of bioturbators on the community diversity of free-living organisms have both been reported and depend on the bioturbating species (Posey et al. 1991, Dittmann 1996, Kanaya 2014). Mouritsen & Haun (2008) evaluated how parasitism interferes with the role of the bioturbating gastropod *P. ulvae* as an EES. Parasitized snails have a negative impact on primary producers whereas unparasitized organisms enhance primary production. The authors suggest that the sediment mixing activity of parasitized snails is reduced, lowering nutrient supply to benthic primary producers. Faunal community structure is also different in sediment bioturbated by parasitized and unparasitized snails, probably because of trophic cascading effects.

## 5.2. Density-mediated effects

The effect of bioturbators as EES relies on their activities but also on their abundance. Therefore, parasites can affect ecosystem functioning *via* density effects on major EES (Mouritsen & Poulin 2002; Poulin 1999) as bioturbators (Fig. 5). We reported several examples of parasites reducing the fecundity and/or the survival of their host (ESMs 2 and 3). The intensity of the bioturbation activity can vary according to population biomass and bioturbator density
369 (e.g., Duport et al. 2006; Sandwell et al. 2009; Braeckman et al. 2010), with potential impacts on 370 ecosystem functioning (Fig. 5). As an illustration, Lohrer et al. (2004) evaluated the influence of 371 a declining density of the irregular urchin *Echinocardium* sp. on nutrient cycling. They 372 highlighted a positive influence of density of urchins on ammonium efflux, and on oxygen, nitrite 373 and nitrate and phosphorus influxes at the sediment-water interface. These nutrients being of 374 fundamental importance for primary production, the microphytobenthic primary production 375 increased with the density of *Echinocardium* sp.. Considering the intricate link between 376 bioturbators and microphytobenthos, one would expect that the reduction of the abundance of 377 bioturbators related to parasitic infection could be ecologically relevant (Fig. 5).

378 Parasites can also interfere with the engineering role of their bioturbating hosts by shaping 379 the size structure of their host populations. Concomitantly, the magnitude of the bioturbation 380 activities of organisms depends on their individual size (Bachteram et al. 2005; Bosch et al. 381 2015). In a laboratory experiment, Bosch et al. (2015) evaluated the influence of the nereid 382 polychaete *Alitta (Neanthes) succinea* biomass on nitrogen cycling by manipulating the density 383 and size of worms. They found that at similar density, large polychaetes (high biomass) 384 stimulated nitrogen solute fluxes at the sediment-water interface to a greater extent than small 385 worms (low biomass). Moreover, large organisms enhanced solute diffusion in deeper horizons 386 of the sediment column compared to small worms. This pattern is probably the result of larger 387 organisms building larger and deeper burrows than small organisms (Davey 1994), which would 388 boost bioirrigation processes (Bosch et al. 2015; Mermillod-Blondin et al. 2004). These examples 389 suggest that parasites could also theoretically interfere with the role of bioturbators in nutrient 390 cycling and/or in shaping benthic environments (*via* reduction of sediment reworking) by 391 modifying the size structure of the population of their bioturbating hosts (Fig. 5).
Finally, it should be considered that parasites can have both trait-mediated and density effects on their bioturbating host. In particular, we documented that the bioturbators identified in this review host a large variety of parasites with complex life cycles (ESM 2 and 3), many of which need to be trophically transmitted (i.e., Platyhelminthes or Acanthocephala) to definitive hosts to reproduce. To facilitate their trophic transmission, parasites can drive significant modifications of behaviour similar to those reported previously for the cockle *A. stutchburyi* (i.e. reduced ability to burry, lower crawling activity). Therefore, such parasite species induce changes in bioturbating host traits and density, altering the functional role of the bioturbator host and ecosystem properties.

### 5.3. What next?

Over the last years, there has been a growing interest in developing indexes providing estimation of the impact of benthic community in the functioning of marine ecosystem. Among them, community bioturbation potential ($BP_c$) and community bioirrigation potential ($BIP_c$) are two metrics estimating the influence of benthic organisms on sediment mixing and solute exchanges, respectively (Renz et al. 2018; Solan et al. 2004; Wrede et al. 2018). Both of these scoring systems rely on a classification of marine infauna based on the (1) abundance, (2) biomass and (3) functional traits of organisms. For instance, the $BIP_c$ categorized species according to their feeding type, burrow type and burrowing depth. Our literature review highlights that parasites modulate the abundance, biomass and functional traits of their bioturbating hosts. For instance, mud shrimp *U. cf. pusilla* parasitized with the bopyrid *G. branchialis* show reduced ventilation rate and built smaller burrow than uninfected organisms. This has consequences on the influence of mud shrimp in driving solute exchange at the sediment-water interface (Pascal 2017). Thus, one would expect that the application of the $BIP_c$
on macrofaunal communities dominated by the mud shrimp *U. cf. pusilla* without taking into account the presence of this parasite conducts to overestimation of the BIPc of such communities, with potential biases in the comparison of ecosystems. In our opinion, a successful application of trait-based indices such as the BPc and the BIPc would gain to take into account (1) the impact of parasites on their bioturbating hosts and (2) the prevalence of parasites in community of bioturbators.

## 6. CONCLUSION

The structure and function of benthic environments is substantially shaped by major ecosystem engineer species (Jones et al. 1994) such as bioturbators (e.g., Krantzberg 1985; Levinton 1995). These organisms play a key role in the physical structure of sediments, on their sediment biogeochemical properties and in nutrient cycling through intense sediment reworking and bioirrigation activities (e.g., Jones & Jago 1993; Rhoads & Young 1970; Volkenborn et al. 2007; Webb & Eyre 2004). When abundant, bioturbators strongly influence the community structure of free-living organisms (e.g., Dahlgren et al. 1999; Pillay et al. 2007; Widdicombe et al. 2000) (Fig. 5). The impact of bioturbators on ecosystem functioning is related to (1) the intensity of their bioturbation and inherently on their physiological state and (2) their abundance. Several factors can interfere with the role of bioturbators as EES (e.g., Duport et al. 2006; Premo & Tyler 2013; Przeslawski et al. 2009), such as parasitism. Parasites are widespread in natural environments (Dobson et al. 2008), but so far only a small proportion of bioturbators have been studied in this regard. We pointed out the deficit of data on parasitism in bioturbating organisms. Moreover, we showed that few studies evaluated the influence of parasites on bioturbating organisms. Among these studies, parasites have been documented to strongly impair the physiological status, fecundity, behaviour and survival of their host. By doing so, parasites
certainly reduce the bioturbation activity of their host. Due to the impact of parasites on their bioturbating hosts and the fact that parasites can be highly prevalent in bioturbating host populations, parasites could have impacts on ecosystem functioning through cascading effects (Fig. 5). In fact, parasites should be considered EES (Thomas et al. 1999) just as bioturbating species are. Therefore, we strongly suggest that parasitism be taken into account when evaluating the role of bioturbators as ecosystem engineers.
444 Acknowledgments

445 A.D. was supported by a doctoral grant of the French “Ministère de l’Enseignement Supérieur et de la

446 Recherche” (Université de Bordeaux - 2015/AUN/25). The authors are grateful to Dr. M.A. Goedknegt for

447 interesting comments on an earlier draft of the manuscript. Many thanks to Dr. R.B. Carnegie (Virginia

448 Institute of Marine Science) for editing the manuscript.
449 **Bibliography**

450 Aller RC. 1982. The effects of macrobenthos on chemical properties of marine sediment and

451 overlying water. In *Animal-Sediment Relations*, Vol. 100, eds. PL McCall, MJS Tevesz, pp. 53–

452 102. Boston, MA: Springer US

453 Aller RC. 1988. Benthic fauna and biogeochemical processes in marine sediments: the role of

454 burrow structures. In *Nitrogen Cycling in Coastal Marine Environments*, pp. 301–38. T. H.

455 Blackburn and J. Sorensen. Wiley ed.

456 Anderson G. 1977. The effects of parasitism on energy flow through laboratory shrimp

457 populations. *Mar. Biol.* 42:239–51

458 Anderson RM, May RM. 1979. Population biology of infectious diseases: Part I. *Nature*.

459 280(5721):361–67

460 Bachteram AM, Mazurek KA, Ciborowski JJH. 2005. Sediment suspension by burrowing

461 mayflies (*Hexagenia* spp., Ephemeroptera: Ephem器idae). *J. Gt. Lakes Res.* 31:208–22

462 Berkenbusch K, Rowden AA. 1999. Factors influencing sediment turnover by the burrowing

463 ghost shrimp *Callianassa filholi* (Decapoda: Thalassinidea). *J. Exp. Mar. Biol. Ecol.* 238(2):283–

464 92

465 Bosch J, Cornwell J, Kemp W. 2015. Short-term effects of nereid polychaete size and density on

466 sediment inorganic nitrogen cycling under varying oxygen conditions. *Mar. Ecol. Prog. Ser.*

467 524:155–69

468 Braeckman U, Provoost P, Gribsholt B, Van Gansbeke D, Middelburg J, et al. 2010. Role of

469 macrofauna functional traits and density in biogeochemical fluxes and bioturbation. *Mar. Ecol. Prog. Ser.* 399:173–86

470 *Prog. Ser.* 399:173–86

471 Caira JN, Littlewood DTJ. 2013. Worms, Platyhelminthes. In *Encyclopedia of Biodiversity*

472 (Second Edition), ed. SA Levin, pp. 437–69. Waltham: Academic Press

473 Campbell BR, Lindsay SM. 2014. Effects of injury and nutrition on sediment reworking by

474 *Clymenella torquata* (Annelida: Polychaeta). *J. Mar. Res.* 72(5):307–29

475 Carballal MJ, Iglesias D, Santamarina J, Ferro-Soto B, Villalba A. 2001. Parasites and pathologic

476 conditions of the cockle *Cerastoderma edule* populations of the coast of Galicia (NW Spain). *J.*

477 *Invertebr. Pathol.* 78(2):87–97

478 Combes C. 1991. Ethological aspects of parasite transmission. *Am. Nat.* 138(4):866–80

479 Combes C. 1995. *Interactions Durables: Écologie et Évolution Du Parasitisme*. Paris: Masson

480 Dahlgren CP, Posey MH, Hulbert AW. 1999. The effects of bioturbation on the infaunal

481 community adjacent to an offshore hardbottom reef. *Bull. Mar. Sci.* 64(1):21–34

482 Dang C, de Montaudouin X, Bald J, Jude F, Raymond N, et al. 2009. Testing the enemy release

483 hypothesis: trematode parasites in the non-indigenous Manila clam *Ruditapes philippinarum*.
484 *Hydrobiologia*. 630(1):139-48

485 Dang C, de Montaudouin X, Binias C, Salvo F, Caill-Milly N, et al. 2013. Correlation between
486 perkinsosis and growth in clams *Ruditapes* spp. *Dis. Aquat. Organ*. 106(3):255-65

487 Dang C, de Montaudouin X, Gonzalez P, Mesmer-Dudons N, Caill-Milly N. 2008. Brown muscle
disease (BMD), an emergent pathology affecting Manila clam *Ruditapes philippinarum* in
489 Arcachon Bay (SW France). *Dis. Aquat. Organ.* 80:219-28

490 Davey JT. 1994. The architecture of the burrow of *Nereis diversicolor* and its quantification in
relation to sediment-water exchange. *J. Exp. Mar. Biol. Ecol.* 179(1):115-29

492 de Montaudouin X, Blanchet H, Kisielewski I, Desclaux C, Bachelet G. 2003. Digenean
trematodes moderately alter *Hydrobia ulvae* population size structure. *J. Mar. Biol. Assoc. U. K.*
83(2):297-305

495 Dittmann S. 1996. Effects of macrobenthic burrows on infaunal communities in tropical tidal flats. *Mar. Ecol. Prog. Ser.* 134:119-30

497 Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W. 2008. Homage to Linnaeus: How many parasites? How many hosts? *Proc. Natl. Acad. Sci.* 105(Supplement 1):11482-89

499 Dumbauld BR, Chapman JW, Torchin ME, Kuris AM. 2011. Is the collapse of mud shrimp
500 (*Upogebia pugettensis*) populations along the Pacific coast of North America caused by
501 outbreaks of a previously unknown bopyrid isopod parasite (*Orthione griffenis*)? *Estuaries
502 Coasts.* 34(2):336-50

503 Duport E, Stora G, Tremblay P, Gilbert F. 2006. Effects of population density on the sediment
mixing induced by the gallery-diffusor *Hediste (Nereis) diversicolor* O.F. Müller, 1776. *J. Exp.
505 Mar. Biol. Ecol.* 336(1):33-41

506 Ewald PW. 1980. Evolutionary biology and the treatment of signs and symptoms of infectious
disease. *J. Theor. Biol.* 86(1):169-76

508 Flye-Sainte-Marie J, Pouvreau S, Paillard C, Jean F. 2007. Impact of Brown Ring Disease on the
energy budget of the Manila clam *Ruditapes philippinarum*. *J. Exp. Mar. Biol. Ecol.* 349(2):378-
89

511 Fredensborg BL, Mouritsen KN, Poulin R. 2004. Intensity-dependent mortality of *Paracalliope novizealandia* (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. *J. Exp. Mar. Biol. Ecol.* 311:253-56

514 Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. 2002. Climate warming and
disease risks for terrestrial and marine biota. *Science.* 296(5576):2158-62

516 Hughes TE. 1940. The effects on the fat and starch metabolism of Gebia by the parasite *Gyge branchialis*. *J. Exp. Biol.* 17(3):331-36

518 Hurd H. 1990. Physiological and behavioural interactions between parasites and invertebrate
hosts. In *Advances in Parasitology*, Vol. 29, pp. 271-318. Elsevier
520 Jensen KT, Mouritsen KN. 1992. Mass mortality in two common soft-bottom invertebrates,

521 *Hydrobia ulvae* and *Corophium volutator* - the possible role of trematodes. *Helgoländer*

522 *Meeresunters.* 46:329–39

523 Jones CG, Lawton JH, Shachak M. 1994. Organisms as Ecosystem Engineers. *Oikos*. 69(3):373

524 Jones CG, Lawton JH, Shachak M. 1997. Positive and negative effects of organisms as physical

525 ecosystem engineers. *Ecology*. 78(7):1946–57

526 Jones SE, Jago CF. 1993. *In situ* assessment of modification of sediment properties by burrowing

527 invertebrates. *Mar. Biol.* 115(1):133–42

528 Jonsson PR, André C. 1992. Mass mortality of the bivalve *Cerastoderma edule* on the swedish

529 west coast caused by infestation with the digenean trematode *Cercariae cerastodermae* I.

530 *Ophelia*. 36:151–57

531 Kamiya T, O'Dwyer K, Nakagawa S, Poulin R. 2014. What determines species richness of

532 parasitic organisms? A meta-analysis across animal, plant and fungal hosts: Determinants of

533 parasite species richness. *Biol. Rev.* 89(1):123–34

534 Kanaya G. 2014. Effects of infaunal bivalves on associated macrozoobenthic communities in

535 estuarine soft-bottom habitats: A bivalve addition experiment in a brackish lagoon. *J. Exp. Mar.*

536 *Biol. Ecol.* 457:180–89

537 Krantzberg G. 1985. The influence of bioturbation on physical, chemical and biological

538 parameters in aquatic environments: A review. *Environ. Pollut. Ser. Ecol. Biol.* 39(2):99–122

539 Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT. 2012.

540 What is bioturbation? The need for a precise definition for fauna in aquatic sciences. *Mar. Ecol.*

541 *Prog. Ser.* 446:285–302

542 Lafferty KD. 1999. The evolution of trophic transmission. *Parasitol. Today*. 15(3):111–15

543 Lauckner G. 1980. Diseases of Mollusca: Gastropoda. In *Diseases of Marine Animals*, Vol. I, pp.

544 311–424. Chichester: Otto Kinne. John Wiley & Sons ed.

545 Lauckner G. 1983. Diseases of Mollusca: Bivalvia. In *Diseases of Marine Animals*, Vol. II, pp.

546 477–961. Hamburg: Otto Kinne. Biologische Anstalt Helgoland ed.

547 Levinton J. 1995. Bioturbators as ecosystem engineers: Control of the sediment fabric, inter-

548 individual interactions, and material fluxes. In *Linking Species & Ecosystems*, eds. CG Jones, JH

549 Lawton, pp. 29–36. Boston, MA: Springer US

550 Lohrer AM, Thrush SF, Gibbs MM. 2004. Bioturbators enhance ecosystem function through

551 complex biogeochemical interactions. *Nature*. 431(7012):1092–95

552 Maire O, Duchêne JC, Grémare A, Malyuga VS, Meysman FJR. 2007. A comparison of sediment

553 reworking rates by the surface deposit-feeding bivalve *Abra ovata* during summertime and

554 wintertime, with a comparison between two models of sediment reworking. *J. Exp. Mar. Biol.*

555 *Ecol.* 343(1):21–36
556 Maire O, Merchant JN, Bulling M, Teal LR, Grémare A, et al. 2010. Indirect effects of non-lethal predation on bivalve activity and sediment reworking. *J. Exp. Mar. Biol. Ecol.* 395(1–2):30–36

558 Marcogliese DJ. 2001. Implications of climate change for parasitism of animals in the aquatic environment. *Can. J. Zool.* 79(8):1331–52

560 Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA. 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American society of parasitologists). *J. Parasitol.* 68(1):131

563 Mautner SI, Cook KA, Forbes MR, McCurdy DG, Dunn AM. 2007. Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod. *Parasitology*. 134:1567–73

565 McLaughlin SM, Faisal M. 1998. Histopathological alterations associated with *Perkinsus* spp. infection in the softshell clam *Mya arenaria*. *Parasite*. 5(3):263–71

567 Mermillod-Blondin F, Rosenberg R. 2006. Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. *Aquat. Sci.* 68(4):434–42

569 Mermillod-Blondin F, Rosenberg R, François-Carcaillet F, Norling K, Mauclaire L. 2004. Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. *Aquat. Microb. Ecol.* 36:271–84

572 Meysman F, Middelburg J, Heip C. 2006. Bioturbation: a fresh look at Darwin’s last idea. *Trends Ecol. Evol.* 21(12):688–95

574 Minchella DJ, Scott ME. 1991. Parasitism: a cryptic determinant of animal community structure. *Trends Ecol. Evol.* 6(8):250–54

576 Moore J. 2002. *Parasites and the Behavior of Animals*. Oxford: Janice Moore. Oxford University Press ed.

578 Mouritsen KN. 2004. Intertidal facilitation and indirect effects: causes and consequences of crawling in the New Zealand cockle. *Mar. Ecol. Prog. Ser.* 271:207–20

580 Mouritsen KN, Haun SCB. 2008. Community regulation by herbivore parasitism and density: Trait-mediated indirect interactions in the intertidal. *J. Exp. Mar. Biol. Ecol.* 367(2):236–46

582 Mouritsen KN, Jensen KT. 1994. The enigma of gigantism: effect of larval trematodes on growth, fecundity, egestion and locomotion in *Hydrobia ulvae* (Pennant) (Gastropoda: Prosobranchia). *J. Exp. Mar. Biol. Ecol.* 181(1):53–66

585 Mouritsen KN, Poulin R. 2002. Parasitism, community structure and biodiversity in intertidal ecosystems. *Parasitology*. 124(07):S101–17

587 Mouritsen KN, Poulin R. 2005. Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. *Oikos*. 108(2):344–50

589 Mouritsen KN, Poulin R. 2010. Parasitism as a determinant of community structure on intertidal flats. *Mar. Biol.* 157(1):201–13
591 Nam K-W, Jeung H-D, Song J-H, Park K-H, Choi K-S, Park K-I. 2018. High parasite burden increases the surfacing and mortality of the Manila clam (*Ruditapes philippinarum*) in intertidal sandy mudflats on the west coast of Korea during hot summer. *Parasit. Vectors.* 11(1):

594 Nates SF, Felder DL. 1998. Impacts of burrowing ghost shrimp, genus *Lepidophthalmus* 595 Crustacea: Decapoda: Thalassinidea, on penaeid shrimp culture. *J. World Aquac. Soc.* 29(2):188–210

597 O’Connell-Milne SA, Poulin R, Savage C, Rayment W. 2016. Reduced growth, body condition 598 and foot length of the bivalve *Austrovenus stutchburyi* in response to parasite infection. *J. Exp. 599 Mar. Biol. Ecol.* 474:23–28

600 Ouellette D, Desrosiers G, Gagne J, Gilbert F, Poggiale J, et al. 2004. Effects of temperature on 601 *in vitro* sediment reworking processes by a gallery biodiffusor, the polychaete *Neanthes virens*. 602 *Mar. Ecol. Prog. Ser.* 266:185–93

603 Pascal L. 2017. *Rôle de l’espèce ingénieure Upogebia pusilla dans le fonctionnement 604 biogéochimique des écosystèmes intertidaux à herbier (Zostera noltei) du bassin d’Arcachon.* 605 University of Bordeaux

606 Pascal L, de Montaudouin X, Grémare A, Maire O. 2016. Dynamics of the *Upogebia pusilla–* 607 *Gyge branchialis* marine host–parasite system. *Mar. Biol.* 163(9):

608 Paul-Pont I, Gonzalez P, Baudrimont M, Jude F, Raymond N, et al. 2010. Interactive effects of 609 metal contamination and pathogenic organisms on the marine bivalve *Cerastoderma edule*. *Mar. 610 Pollut. Bull.* 60(4):515–25

611 Pearre S. 1976. Gigantism and partial parasitic castration of Chaetognatha infected with larval 612 trematodes. *J. Mar. Biol. Assoc. U. K.* 56(02):503

613 Pérez Camacho A, Villalba A, Beiras R, Labarta U. 1997. Absorption efficiency and condition of 614 cultured mussels (*Mytilus edulis galloprovincialis* Linnaeus) of Galicia (NW Spain) infected by 615 parasites *Marteilia refringens* Grizel et al. and *Mytilicola intestinalis* Steuer. *J. Shellfish Res.* 616 16(1):77–82

617 Pillay D, Branch GM, Forbes AT. 2007. Experimental evidence for the effects of the 618 thalassinidean sandprawn *Callianassa kraussi* on macrobenthic communities. *Mar. Biol.* 619 152(3):611–18

620 Posey MH, Dumbauld BR, Armstrong DA. 1991. Effects of a burrowing mud shrimp, *Upogebia* 621 *pugettensis* (Dana), on abundances of macro-infauna. *J. Exp. Mar. Biol. Ecol.* 148(2):283–94

622 Poulin R. 1999. The functional importance of parasites in animal communities: many roles at 623 many levels? *Int. J. Parasitol.* 29(6):903–14

624 Premo K, Tyler A. 2013. Threat of predation alters the ability of benthic invertebrates to modify 625 sediment biogeochemistry and benthic microalgal abundance. *Mar. Ecol. Prog. Ser.* 494:29–39

626 Preston DL, Mischler JA, Townsend AR, Johnson PTJ. 2016. Disease ecology meets ecosystem
627 science. *Ecosystem*. 19(4):737-48

628 Price PW, Wastoby M, Rice B, Atsatt PR, Fritz RS, et al. 1986. Parasite mediation in ecological

629 interactions. *Annu. Rev. Ecol. Syst.* 17:487-505

630 Probst S, Kube J. 1999. Histopathological effects of larval trematode infections in mudsnails and

631 their impact on host growth: what causes gigantism in *Hydrobia ventrosa* (Gastropoda:

632 Prosobranchia)? *J. Exp. Mar. Biol. Ecol.* 238(1):49-68

633 Przeslawski R, Zhu Q, Aller R. 2009. Effects of abiotic stressors on infaunal burrowing and

634 associated sediment characteristics. *Mar. Ecol. Prog. Ser.* 392:33-42

635 Reinhard EG. 1956. Parasitic castration of crustacea. *Exp. Parasitol.* 5(1):79-107

636 Renz JR, Powilleit M, Gogina M, Zettler ML, Morys C, Forster S. 2018. Community

637 bioirrigation potential (BIPc), an index to quantify the potential for solute exchange at the

638 sediment-water interface. *Mar. Environ. Res.* 141:214-24

639 Repetto M, Griffen BD. 2012. Physiological consequences of parasite infection in the burrowing

640 mud shrimp, *Upogebia pugettensis*, a widespread ecosystem engineer. *Mar. Freshw. Res.*

641 63(1):60

642 Rhoads DC, Young DK. 1970. The influence of deposit-feeding organisms on sediment stability

643 and community trophic structure. *J. Mar. Res.* 28(2):150-78

644 Robaldo RB, Monserrat J, Cousin JCB, Bianchini A. 1999. Effects of metacercariae (Digenea:

645 Microphallidae) on the hepatopancreas of *Chasmagnathus granulata* (Decapoda: Grapsidae). *Dis.*

646 Aquat. Organ.* 37:153-57

647 Rohde K. 2005. *Marine Parasitology*. Australia. CSIRO ed.

648 Sandwell DR, Pilditch CA, Lohrer AM. 2009. Density dependent effects of an infaunal

649 suspension-feeding bivalve (*Austrovenus stutchburyi*) on sand flat nutrient fluxes and

650 microphytobenthic productivity. *J. Exp. Mar. Biol. Ecol.* 373:16-25

651 Simão MF, Leite RB, Rocha C, Cancela ML. 2010. Changes in bioturbation of iron

652 biogeochemistry and in molecular response of the clam *Ruditapes decussates* upon *Perkinsus*

653 *olseni* infection. *Arch. Environ. Contam. Toxicol.* 59(3):433-43

654 Sluiters JF, Brussaard-Wüst CM, Meuleman EA. 1980. The relationship between miracidial dose,

655 production of cercariae, and reproductive activity of the host in the combination *Trichobilharzia*

656 *ocellata* and *Lymnaea stagnalis*. *Z. Für Parasitenkd. Parasitol. Res.* 63(1):13-26

657 Smith AE, Chapman JW, Dumbauld BR. 2008. Population structure and energetics of the bopyrid

658 isopod parasite *Orthione griffenis* in mud shrimp *Upogebia pugettensis*. *J. Crustac. Biol.*

659 28(2):228-33

660 Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS. 2004.

661 Extinction and ecosystem function in the marine benthos. *Science*. 306(5699):1177-80
662 Stier T, Drent J, Thieltgès DW. 2015. Trematode infections reduce clearance rates and condition
663 in blue mussels *Mytilus edulis*. *Mar. Ecol. Prog. Ser.* 529:137–44

664 Studer A, Poulin R. 2013. Differential effects of temperature variability on the transmission of a
665 marine parasite. *Mar. Biol.* 160(10):2763–73

666 Thieltgès DW. 2006. Parasite induced summer mortality in the cockle *Cerastoderma edule* by the
667 trematode *Gymnophallus choledochus*. *Hydrobiologia.* 559(1):455–61

668 Thomas F, Poulin R. 1998. Manipulation of a mollusc by a trophically transmitted parasite:
669 convergent evolution or phylogenetic inheritance? *Parasitology*. 116(5):431–36

670 Thomas F, Poulin R, de Meeus T, Guegan J-F, Renaud F. 1999. Parasites and ecosystem
671 engineering: what roles could they play? *Oikos*. 84(1):167–71

672 Thomas F, Renaud F, de Meeûs T, Poulin R. 1998. Manipulation of host behaviour by parasites:
673 ecosystem engineering in the intertidal zone? *Proc. R. Soc. B Biol. Sci.* 265:1091–96

674 Tucker BW. 1930. Memoirs: on the effects of an epicaridan parasite, *Gyge branchialis*, on
675 *Upogebia littoralis*. *J. Cell Sci.* s2-74(293):1–118

676 Villalba A, Iglesias D, Ramilo A, Darriba S, Parada J, et al. 2014. Cockle *Cerastoderma edule*
677 fishery collapse in the Ría de Arousa (Galicia, NW Spain) associated with the protistan parasite
678 *Marteilia cochillia*. *Dis. Aquat. Organ.* 109(1):55–80

679 Volkenborn N, Hedtkamp SIC, van Beusekom JEE, Reise K. 2007. Effects of bioturbation and
680 bioirrigation by lugworms (*Arenicola marina*) on physical and chemical sediment properties and
681 implications for intertidal habitat succession. *Estuar. Coast. Shelf Sci.* 74(1–2):331–43

682 Volkenborn N, Polerecky L, Wethey D, DeWitt T, Woodin S. 2012. Hydraulic activities by ghost
683 shrimp *Neotrypaea californiensis* induce oxic–anoxic oscillations in sediments. *Mar. Ecol. Prog.
684 Ser.* 455:141–56

685 Webb AP, Eyre BD. 2004. Effect of natural populations of burrowing thalassinidean shrimp on
686 sediment irrigation, benthic metabolism, nutrient fluxes and denitrification. *Mar. Ecol. Prog. Ser.*
687 268:205–20

688 Widdicombe S, Austen MC, Kendall MA, Warwick RM, Jones MB. 2000. Bioturbation as a
689 mechanism for setting and maintaining levels of diversity in subtidal macrobenthic communities.
690 *Hydrobiologia.* 440(1/3):369–77

691 Williams JD, Boyko CB. 2012. The global diversity of parasitic isopods associated with
692 crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). *PLOS ONE*. 7(4):e35350

693 WoRMS Editorial Board. 2018. World Register of Marine Species

694 Wrede A, Beerman J, Dannheim J, Gutow L, Brey T. 2018. Organism functional traits and
695 ecosystem supporting services – A novel approach to predict bioirrigation. *Ecol. Indic.* 91:737–
696 43
698

**Figure**

<figure><img src="image_2.png" /></figure>

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**Fig. 1** Number of coastal bioturbating species commonly studied and number of parasitized bioturbators per taxonomic clade. Parasitized bioturbators are categorized as being infected with macroparasites only, microparasites only or both groups of parasites.

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<figure><img src="image_3.png" /><figcaption>**Fig. 2** Number (log scale axis) of (A) macroparasite and (B) microparasite species identified per bioturbating host species. Bioturbators are classified according to their taxonomic clade. The boxes represent the interquartile range, the black lines the median and the red dots the mean number of parasites species in each clade of bioturbators.</figcaption></figure>
<figure><img src="image_4.png" /></figure>

<figure><img src="image_5.png" /><figcaption>**Fig. 3** Taxonomic types of (A) macroparasites and (B) microparasites reported in clades of bioturbating species. The total number of parasite species identified per clade of bioturbators is given (N).</figcaption></figure>

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

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<caption>**Fig. 4** Impacts of macro- and microparasites on bioturbating organisms. Alterations of physiological state: parasites influencing gene expression, cellular functions, physical integrity, growth rates of the host, etc. Modifications of reproductive functions: parasites reducing or increasing their host's fecundity, causing total or partial castration, etc. Modifications of behaviour: parasites reducing their host's activity levels, inducing abnormal behaviours, etc. Increase of the mortality rate: changes in survival. Total number of studies *N* = 85, of which *N* = 35 studies on macroparasites and *N* = 47 studies on microparasites.</caption>
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<figure><img src="image_7.png" /></figure>

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Fig. 5 Impacts of parasites on bioturbating organisms and on their influence as ecosystem engineer species (EES). The behaviour of bioturbating organisms conditions the intensity of their bioturbation and their role as EES when they are abundant. Parasites can significantly alter the physiological state of organisms with consequences on their behaviour, fecundity and survival. By doing so, parasites can regulate the density of their host population or altered their functional traits. Both density- and trait mediated effects of parasites on bioturbators would modify the functional roles of these organisms as EES.
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<table><caption>**Table 1** Summary of the literature evaluating the influence of parasitism on the activity and the role as ecosystem engineer species of bioturbating species.</caption><thead><tr><td>Bioturbator</td><td>Parasite</td><td>Type of parasite</td><td>Effects of parasitism</td><td>Type of effect</td><td>References</td></tr></thead><tbody><tr><td>Upogebia cf. pusilla</td><td>Gyge branchialis</td><td>Macroparasite: Isopoda</td><td>Moribund organisms<ul><li>4.5-fold lower sediment reworking rate 2.9-fold lower bioirrigation rate</li><li>Reduced influence on nutrient exchanges (TOU, NH<sub>4</sub><sup>+</sup>, NO<sub>3</sub><sup>-</sup>, dSi)</li></ul></td><td>Direct effects leading to trait-mediated effects</td><td>(Pascal 2017)</td></tr><tr><td>Austrovenus stutchburyi</td><td>Curtuteria australis</td><td>Macroparasite: Trematoda</td><td>Changes in the epibiont community of cockles<ul><li>The authors hypothesizing that the parasite interfering with the ability of cockles to burrow (Thomas & Poulin 1998) modifies their role as autogene engineers.</li></ul></td><td>Trait-mediated effects</td><td>(Thomas et al. 1998)</td></tr><tr><td>Austrovenus stutchburyi</td><td>Curtuteria australis</td><td>Macroparasite: Trematoda</td><td>Reduced crawling activity (mean distance travelled) of highly infected cockles (the cockles' crawling activity considered to be a measure of their bioturbation potential)</td><td>Direct effect</td><td>(Mouritsen 2004)</td></tr><tr><td>Austrovenus stutchburyi</td><td>Curtuteria australis</td><td>Macroparasite: Trematoda</td><td>Changes in the structure of the intertidal benthic community: increased abundances of some macroinvertebrates, modifications of the biomass of certain taxonomic groups, increased species diversity.<ul><li>The authors hypothesizing that parasitism reduces the mobility of cockles (1) lowering the sediment disturbance and (2) providing new colonisable substrate (see Thomas et al. 1998)</li></ul></td><td>Trait-mediated effects</td><td>(Mouritsen & Poulin 2010)</td></tr><tr><td>Austrovenus stutchburyi</td><td>Echinostome trematodes (genera Curtuteria + Acanthoparyphiu m)</td><td>Macroparasite: Trematoda</td><td>Reduced crawling activity (mean distance travelled) of highly infected cockles, meaning the disturbance of the upper sediment layer is relaxed<ul><li>Changes in the structure of the intertidal benthic community: increase of the total abundance of macroinvertebrates and of the species richness</li></ul></td><td>Direct effects leading to trait-mediated effects</td><td>(Mouritsen & Poulin 2005)</td></tr></tbody></table>
Reduced burrowing capability

➤ Changes in the structure of the intertidal benthic community: increase of the density of certain macroinvertebrates, modification of the taxonomical composition of the benthic community.

➤ Changes in sediment characteristics and seabed elevation.

<table><tr><td><strong>Peringia (Hydrobia) ulvae</strong></td><td><em>Cryptocotyle concave</em> or <em>Himasthla</em> spp. or <em>Maritrema</em> spp. Or <em>Microphallus claviformis</em></td><td>Macroparasite: Trematoda</td><td>No effect on sediment characteristics (organic content, median particle diameter, sorting coefficient, ...)<br/>Decrease of the chlorophyll-a content of the sediment<br/>Changes in the diatom community structure (epipelic and epipsammic diatoms)<br/>Changes in the structure of the intertidal benthic community: increased abundances of some invertebrates while the abundances of others decreased<br/>➤ The authors hypothesizing that parasitism reduces the mobility of snails (Mouritsen & Jensen 1994), lowering the sediment disturbance. Thus, there is a decrease of the release of nutrients leading to a decline in the microphytobenthos biomass. This is associated to a decrease of the diversity of some primary producers and an increase diversity of few secondary producers.</td><td>Trait-mediated effects</td><td>(Mouritsen & Haun 2008)</td></tr><tr><td><strong>Ruditapes decussatus</strong></td><td><em>Perkinsus olseni</em></td><td>Microparasite: Myzozoa</td><td>Reduced impact on iron mobilization (but this appears to depend on the clam density).<br/>➤ The authors hypothesizing that the infection impacts the physiology of clams with organisms being lethargic.</td><td>Trait-mediated effects</td><td>(Simão et al. 2010)</td></tr></table>