# A small increase in temperature could rapidly expand the latitudinal range and pathogenicity of the marine trematode parasite *Curtuteria arguinae*

Leslie Stout, Itsaso Lopez-Ahedo, Guillemine Daffe, Aurélie Chambouvet, Xavier De Montaudouin

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Leslie Stout, Itsaso Lopez-Ahedo, Guillemine Daffe, Aurélie Chambouvet, Xavier De Montaudouin. A small increase in temperature could rapidly expand the latitudinal range and pathogenicity of the marine trematode parasite *Curtuteria arguinae*. Estuarine, Coastal and Shelf Science, 2025, 326, pp.109541. 10.1016/j.ecss.2025.109541. hal-05346366

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# A small increase in temperature could rapidly expand the latitudinal range and pathogenicity of the marine trematode parasite *Curtuteria arguinae*

Leslie Stout<sup>a, *</sup>, Itsaso Lopez-Ahedo<sup>a, ∗</sup>, Guillemine Daffe<sup>b, †</sup>, Aurélie Chambouvet<sup>c</sup>, Xavier de Montaudouin<sup>a, ‡</sup>

<figure><img src="image_3.png" /></figure>

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ARTICLE INFO

Keywords:

Parasite infection

Temperature

Light

Cerastoderma edule

Climate change

Gastropod

Echinostomatoides

A B S T R A C T

The phenology and transmission dynamics of the marine trematode *Curtuteria arguinae* were investigated, a parasite whose recently elucidated life cycle involves oystercatchers (*Haematopus ostralegus*), needle snails (*Bittium reticulatum*), and edible cockles (*Cerastoderma edule*). To assess the influence of temperature and light on cercarial emergence, infected *B. reticulatum* were exposed to temperatures ranging from 15 °C to 27 °C under both light and dark conditions. Cercarial emergence peaked under warm and illuminated conditions, showing strong temperature dependence, and, to a lesser extent, light dependence. Emergence occurred significantly at temperatures ≥21 °C, with median emergence rates of 12–47 cercariae.day⁻¹, and the positive influence of light was overruled at higher temperatures. A 22-year dataset from Arcachon Bay (France) was also analyzed to determine the timing of first infections in cockles relative to sea and air temperatures, as well as cockle shell size, across ten cohorts. First infections of cockles were consistently observed in late summer, with a mean sea temperature of 20.8 °C, placing cercarial transmission once a thermal threshold is reached. This thermal dependency explains the parasite's current southern distribution. With climate warming, its range is likely to expand northward along the northeastern Atlantic coast, in areas where all hosts are already present. Expansion may also be supported by the northward extension of *B. reticulatum*. In areas where the parasite is already established, rising temperatures may enhance cercarial output and infection intensity, increasing pathogenic effects on both intermediate hosts and posing a growing threat to ecosystem functioning and cockle fisheries.

# 1. Introduction

Among biotic factors, parasitism plays a major role, impacting in-
dividuals, populations (Desclaux et al., 2004; Fredensborg et al., 2005),
communities (Mouritsen and Poulin, 2010; Thieltges et al., 2013), and
ecosystems (Brian et al., 2022; Zander and Reimer, 2002). Trematodes
are the most prevalent and abundant macroparasites in coastal waters
(Lauckner, 1983), representing a significant percentage of marine
biomass (Kuris et al., 2008). They have a complex and heteroxenous life
cycle, generally comprising two or three parasitic and two free-living
stages (Dawes, 2011). Taking the example of the echinostomatid fam-
ily, adult trematodes reside in an avian definitive host, through which
parasite eggs are shed via the digestive tract. After hatching, the mira-
cidium (a free-living larval stage) infects the first intermediate host (a
gastropod) by penetrating its tissue, where it metamorphoses into a
sporocyst and rediae. Here, trematodes multiply asexually and emerge

as cercariae (a free-living stage) that actively swim in search of a second
intermediate host, generally a mollusc or an amphibian. This free-living
larval stage has a short lifespan and must ensure successful transmission
between hosts. In the second intermediate host, the new stage, called
metacercaria, "waits" for the host to be predated upon by the definitive
host to complete the life cycle. This complex life cycle has significant
consequences for parasite distribution. Both parasitic and free-living
stages are directly or indirectly dependent on environmental variables,
particularly temperature. To understand the impact of parasites on their
host populations, it is important to identify the different hosts of their
life cycles, assess their geographic distribution, determine the factors
influencing their occurrence, and predict how their distribution might
be modified in a climate change context.

There are two situations where a parasite displaying a complex life
cycle can be unsuccessful in settling in the environment: 1) when one or
more hosts of the life cycle are missing. This is typically the case in

<footnote><sup>a</sup> University of Bordeaux, CNRS, Bordeaux INP, EPOC, UMR 5805, Station Marine, 33120, Arcachon, France</footnote>

<footnote><sup>b</sup> University of Bordeaux, CNRS, OASU, UAR 2567 POREA, 33615, Pessac, France</footnote>

<footnote><sup>c</sup> Sorbonne Université, CNRS, UMR7144 AD2M, ECOMAP, Station Biologique de Roscoff, 29680, Roscoff, France</footnote>

<footnote>* Corresponding author. 2 rue du Professeur Jolyet, 33120, Arcachon, France.</footnote>

<footnote>E-mail address: leslie.stout@u-bordeaux.fr (L. Stout).</footnote>
species introductions. Usually, non-indigenous species (NIS) pop-
ulations settle in new environments and rapidly lose their native trem-
atode species, which can no longer complete their complex life cycle
(Dang et al., 2009; Kvach and Stepien, 2008). This process, called the
"Enemy Release Hypothesis" (Calvo-Ugarteburu and McQuaid, 1998;
Colautti et al., 2004), occurs because parasites are often specific to their
host and cannot accommodate to a new environment with different
species, benefiting the NIS compared to native species that retain their
native parasites. However, in some rare cases, the species range of po-
tential hosts may be broader than expected. For instance, the trematode
*Bacciger bacciger* typically uses the genus *Donax* (bivalve) as its first in-
termediate host (Palombi, 1934; Ramón et al., 1999), but was recently
found in Korea in the phylogenetically distant species *Ruditapes philip-
pinarum* (Le et al., 2024). Another example for host distribution driving
parasite distribution is *Himasthla elongata* (Echinostomatoidae:
Himasthliidae). This trematode is absent in its second intermediate hosts
(*Cerastoderma edule* and *Mytilus* spp.) in southern Portugal (*Correia
et al., 2020; de Montaudouin et al., 2021*), where temperature is
compatible with infection (Díaz-Morales et al., 2022) and where Larid
migratory birds are certainly infected as definitive hosts, but its first
intermediate host (*Littorina littorea*) is absent. In other words, if appro-
priate environmental conditions, particularly sea temperature, are pre-
sent, but one of the host species required for the life cycle is absent, the
parasite cannot establish. 2) Though potential hosts may be present in a
given area, the parasite is absent or occurs at low intensity, suggesting
that unfavorable environmental conditions may restrict the parasite's
distribution to a narrower range than that of its hosts or, at least, its
intensity and/or prevalence in host populations.

The trematode species *Curtuteria arguinae* (Desclaux, RUssel-Pinto, de Montaudouin and Bachelet, 2006) might illustrate the second scenario described above, where all hosts are present but environmental conditions restrict parasite transmission. This echinostome was first described on Banc d'Arguin, Arcachon Bay, France, in the edible cockle (C. edule) as a second intermediate host (Desclaux et al., 2006), and has since been observed mainly in cockles along the Atlantic coast between France and Morocco (Alfeddy et al., 2024; Correia et al., 2020; de Montaudouin et al., 2021) and occasionally in clams (R. decussatus, R. phillipinarum, Polititapes aureus) (Alfeddy et al., 2024; Dang et al., 2009). In 2025, the complete life cycle of C. arguinae was elucidated, with needle snails (Bittium reticulatum) and European oystercatchers (Haematopus ostralegus) serving as the first intermediate and definitive hosts, respectively (Stout et al., 2025). The shared distribution of these three host species (oystercatcher, needle snail and edible cockle) spans from 20°N (Banc d'Arguin, Mauritania) to 69°N (Norway) (Høisæter, 2009; Honkoop et al., 2008; Tebble, 1966; van de Pol et al., 2014; Wolff et al., 1993). However, C. arguinae is currently known to occur between 23°N (Dakhla, Morocco) and 44°N (Arcachon Bay, France) (Correia et al., 2020; de Montaudouin et al., 2021). This comparison suggests that factors other than host presence may influence the distribution of C. arguinae. In marine systems, the emergence of cercariae from the first intermediate host and subsequent infection of the second intermediate host often depends on three factors with values fluctuating at different temporal scales: temperature (monthly), light (24-h periods), and when applicable, tide/depth (12-h periods) (Fingerut et al., 2003; Prokofiev et al., 2023). The tide plays a significant role in estuaries, where sessile or weakly motile benthic fauna experience fluctuating conditions in salinity, turbidity, and temperature. However, in this field situation (Banc d'Arguin), tidal rhythms do not drastically alter water body characteristics, so attention was given to temperature and, to a lesser extent, light.

This study investigates how temperature and light influence the
emergence and transmission dynamics of *C. arguinae*, using both
controlled experiments and long-term field observations. Specifically,
the study had three main objectives: 1) to measure cercarial emergence
rates from infected *B. reticulatum* across a wide controlled temperature
range (15–27 °C) under dark and light conditions. Given the relatively

low latitude distribution of *C. arguinae*, maximum emergence was ex-
pected at higher temperatures. Similar to other trematodes, emergence
was also expected to vary under different light conditions (Correia et al.,
2021; Lewis et al., 1989; Titi et al., 2014; Toledo et al., 1999); 2) to
detect the first infection of newly recruited cockles by *C. arguinae* during
a 22-year field monitoring. For similar reasons, an infection of newly
recruited cockles (second intermediate host) was expected in late sum-
mer, coinciding with the highest air and sea temperatures; and 3) to
assess how the future distribution and/or pathogenicity of *C. arguinae* in
cockles could be modified in the northeastern Atlantic in a climate
change scenario, particularly with rising sea temperatures. Beyond
better understanding parasite-host dynamics and the phenology of
*C. arguinae*, the study aims to predict future infection patterns in cockles,
which could, under high intensity, lead to cockle mortality (Desclaux
et al., 2006) and impact associated fisheries.

**2. Materials and methods**

2.1. Study area

Molluscs for this study were collected on Banc d'Arguin, Arcachon Bay, France (Fig. 1). Arcachon Bay is a 182-km² semi-enclosed lagoon along the southwest Atlantic coast of France (44°41'N, 1°8'W). Banc d'Arguin, a sand island located at the entrance of the lagoon (Fig. 1), is a national reserve which features semi-sheltered intertidal sandflats that occasionally support a population of cockles. The sediment is primarily composed of sand with a median grain size of 330 µm (de Montaudouin and Lanceleur, 2011). Salinity remains relatively stable, ranging from 34 to 35, while water temperature fluctuates between 9.5 °C in winter and 21.5 °C in summer. The temperature variation in the sediment is more extreme, ranging from -0.2 °C to 32 °C, driven by air temperature during low tide. The tide is semidiurnal, with heights ranging from 0.9 to 4.9 m (Gassiat, 1989).

## 2.2. Cercarial emergence according to temperature and light

2.2.1. Experiment design

In October and November 2023, a total of 991 needle snails (Bittium reticulatum) were collected from a *Zostera noltii* seagrass bed on Banc d'Arguin (44°34.813'N, 1°14.550'W, Fig. 1), using a 2-mm mesh sieve. The snails were placed individually in plexiglass boxes (dimensions: 5.5 cm x 5.5 cm x 2.5 cm) filled with seawater (salinity: 30) and kept at a

<figure><img src="image_4.png" /><figcaption>**Fig. 1.** Location of the sampling site in Arcachon Bay, France, along with the sites where air and sea temperature data were recorded.</figcaption></figure>
temperature of approximately 22 °C for 24 h under light conditions. After this period, each box was examined under a stereomicroscope to check for the presence of *Curtuteria arguinae* cercariae.

A total of 16 snails released *C. arguinae* cercariae, which were identified through morphological characteristics. Shell height was measured from the apex to the base of the shell to the lesser millimeter, using a caliper. Four snails were kept for another study. The twelve remaining snails were tagged and then kept in cooler water (15 °C) for at least seven days prior to experimentation, with fragments of green algae provided as food. Five temperature levels (15 °C, 18 °C, 21 °C, 24 °C, and 27 °C) and two light conditions (light on/off, 13000 lx, 43 W.m⁻²) were tested in a temperature-controlled chamber. The light/dark cycle was set to 12 h of light and 12 h of darkness for experiments conducted in spring, and 15 h of light and 9 h of darkness for early summer experiments. However, all results were adjusted to a standard 12-h light/dark cycle. To minimize the influence of endogenous rhythms (Craig, 1975; Fingerut et al., 2003; Lewis et al., 1989), which could manifest as emergence peaks aligning with the natural periodicity of the rhythm, light periods could begin during either day or night.

Due to the limited number of cercariae-emitting snails, the experiment followed a repeated-measures design, with each of the 12 snails undergoing all treatment conditions. The order of the tested temperatures was randomly selected (21 °C, 18 °C, 24 °C, 15 °C and 27 °C). The snails were individually placed in plexiglass boxes filled with seawater at 15 °C and positioned on a tray in the temperature-controlled chamber for 48 h, alternating between light and dark periods of 12 h as described. After each light or dark period, the snails were transferred to new boxes, and the previous boxes were examined under a stereomicroscope to detect and count *C. arguinae* cercariae. Results from the dark periods were pooled, as were those from the light periods. After each trial, the snails were returned to a holding tank at 15 °C with food for one week before being subjected to a new trial at a different temperature. The median number of cercariae released over a 24-h period by the 12 snails was calculated under both light and dark conditions for the five different temperatures.

### 2.2.2. Statistical analyses

A generalized linear mixed model (GLMM) was used to assess the effects of temperature and light on cercarial emergence. A GLMM was an appropriate tool as it considers a random effect generated by the dependence of the samples (repeated measures on the same snails), and tests for a potential interaction between temperature and light. Temperature and light variables were treated as fixed effects and the snail variable as a random effect. Data distribution showed strong right-skewness (many zeros) and overdispersal. Thus, the model was implemented with a negative binomial distribution appropriate for count data. The snails #6 and #12, which exhibited extreme cercarial counts, were removed from the dataset to homogenize the random effect of snails. As almost no cercariae emerged at 15 °C, this temperature was removed from the dataset for a better fit of the model. The model was thus constructed with a final dataset made up of 80 observations based on 10 snail individuals, according to four levels of temperature and two levels of light conditions. A type III ANOVA was conducted to test for significant effects of the variables and their interaction. Post-hoc tests based on the estimated marginal means were performed to further investigate the variables' effects. Analyses were conducted using the R software (2024.12.1, R Core Team, 2025). The packages "lme4" (Bates et al., 2015), "ggeffects" (Lüdecke, 2018) and "performance" (Lüdecke et al., 2021) were used to conduct the GLMM analysis. The package "car" (Fox and Weisberg, 2019) was used for the ANOVA and "emmeans" (V1.11.0, Lenth, 2025) for the post-hoc tests.

## 2.3. Long-term monitoring of cockle infection

### 2.3.1. Cockle sampling

The population of cockles (*Cerastoderma edule*) was sampled over a 22-year period on Banc d'Arguin (44°34.813'N, 1°14.550'W, Fig. 1).

From January 1998 to December 2019, cockles were collected monthly at low tide using six 0.25-m² quadrats arranged along a 100-m transect parallel to the water's edge, positioned between 0.5 and 2.0 m above the low tide level. Samples were sieved with a 1 mm mesh. Cockles were counted, and the shell length of each individual was measured to the lesser millimeter using calipers. Cockles typically recruit between May and June at Banc d'Arguin (de Montaudouin et al., 2021).

### 2.3.2. Cockle cohort analysis

Monthly length-frequency histograms were analyzed using the Bhattacharya method to differentiate the various cohorts in the cockle dataset (Bhattacharya, 1967). Each cockle cohort was tracked, when possible, for up to five months (May 0+ to September 0+). This analysis was carried out using the software package FISAT II (FAO-ICLARM stock assessment tool II) (Gayanilo et al., 2005). Modal class progression analysis (MPA) was employed to identify cohorts by decomposing the polymodal size distribution into its normal distribution components. Cohorts were considered "existent" when their density was ≥10 individuals per m², and a cohort was deemed singular if the separation index between two consecutive shell size classes was >2 (Gayanilo et al., 2005). In this study, recruits were defined as the first individuals caught by a 1 mm mesh sieve after settling in the sediment.

### 2.3.3. Parasite analysis

*Curtuteria arguinae* metacercariae were identified in all sampled cockles. Each month, ten cockles from each cohort were dissected, placed and squeezed between two glass slides, and observed under a stereomicroscope. The number of dissected cockles and the mean abundance of *C. arguinae* metacercariae per cockle were calculated for each class of cockle shell length. To detect the first infection event in the cockle's life, the abundance of *C. arguinae* was further examined in newly recruited cohorts (0+ cohorts) from May to September. Because erratic infection is possible all year long (Lyholt and Buchmann, 1996), a threshold of five metacercariae per cockle, on average, was set as the baseline infection level over the cockle's lifetime, regardless of the season, to define the first infection date. Due to low infection rates and/or low cockle recruitment in certain years, analyses could only be properly conducted on 10 out of the 22 initial cohorts (1998-99, 2002-03, 2007-09, 2011-12, and 2014).

### 2.3.4. Environmental data acquisition

At the date corresponding to mid-term between two cockle sampling occasions, cockle shell lengths, mean sea temperatures, and mean maximum daily air temperatures were calculated between two cockle sampling occasions. Air temperature data were obtained from Meteo France (https://donneespubliques.meteofrance.fr/) at a station located 7 km from the cockle sampling site on Banc d'Arguin (44°34.085'N, 1°14.467'W, Fig. 1), where data were recorded every minute. The daily maximum temperatures were selected, and the mean of these values was calculated for the period between each cockle sampling date from May to September, the critical period for the first cockle infection by *C. arguinae*. Water temperature data between May and September for each year were obtained from the ARCHYD program (https://wwz.ifremer.fr/Recherche/Departements-scientifiques/Focus/Quadrigue). The monitoring station for this program was located 1.5 km from the cockle sampling area (44°37.800'N, 1°15.000'W, Fig. 1), within the same water mass (the external neritic water body). In this program, monthly measurements are typically done on four different dates, two at low tide and two at high tide. The mean sea temperature (°C) between cockle sampling dates was calculated based on the four values. All plots were created using the package "ggplot2" (Wickham, 2016) in R.
<figure><img src="image_5.png" /><figcaption>**Fig. 2.** Abundance of *Curtuteria arguinae* cercariae emerged from twelve *Bittium reticulatum* individuals over 24-h periods in both light and darkness, across five water temperatures.</figcaption></figure>
<caption>**Table 1**</caption>

Minimum, maximum, and median number of emerged *Curtuteria arguinae* cercariae from individual *Bittium reticulatum*, and number of snails releasing cercariae under different temperature and light conditions.

<table><thead><tr><th>Light condition</th><th>Temperature (°C)</th><th>Min-Max number of cercariae</th><th>Median number of cercariae</th><th>Snails releasing cercariae</th></tr></thead><tbody><tr><td rowspan="5">Light</td><td>15</td><td>0–6</td><td>0.0</td><td>5</td></tr><tr><td>18</td><td>0–42</td><td>0.0</td><td>4</td></tr><tr><td>21</td><td>0–159</td><td>10.8</td><td>10</td></tr><tr><td>24</td><td>0–68</td><td>8.3</td><td>11</td></tr><tr><td>27</td><td>1–94</td><td>19.5</td><td>12</td></tr><tr><td rowspan="5">Dark</td><td>15</td><td>0–0</td><td>0.0</td><td>0</td></tr><tr><td>18</td><td>0–29</td><td>0.0</td><td>2</td></tr><tr><td>21</td><td>0–43</td><td>0.5</td><td>6</td></tr><tr><td>24</td><td>0–319</td><td>2.7</td><td>6</td></tr><tr><td>27</td><td>0–229</td><td>17.3</td><td>8</td></tr></tbody></table>

# 3. Results

## 3.1. Experimental cercarial emergence

Sieved through a 2-mm mesh, a total of 16 infected needle snails were obtained out of a total of 991 individuals. This represents, for this shell height class and considering snails releasing cercariae, a prevalence of 1.6 %. Infected shell height ranged from 9.8 to 11.9 mm, with a mean of 10.7 mm.

During the experiments, cercarial emergence rates showed significant individual variability. Some snails released more than 100 cercariae over a 24-h period (e.g., snails #9, #11, and #12), while others released no more than five cercariae in the same time frame (e.g., snails #2, #3, and #6) (Fig. 2). At 15 °C and 18 °C, a maximum of five snails in light and six in darkness released cercariae out of the 12 tested (Table 1). At these temperatures, the median cercariae abundance was null (Fig. 3), although a peak of 42 cercariae was observed at 18 °C from snail #12. Overall, an increasing trend in cercariae abundance with

rising temperature was observed, with the lowest abundance at 15 °C (median = 0) and the highest abundance at 27 °C (median = 17.3 and 19.5 in dark and light condition respectively) (Table 1). In light, cercariae emerged mostly between 21 °C and 27 °C, with nearly all snails releasing cercariae in this temperature range (Table 1 and Fig. 3). In darkness, half of the snails released cercariae at 21 °C and 24 °C, but the median emergence rate was six times lower than that observed in light. At 27 °C however, the median cercariae abundance in darkness was not much different from that in light (Fig. 3), although fewer snails released

<caption>**Table 2**</caption>

Significance of the effects of temperature and light on cercariae abundance based on the GLMM model (type III ANOVA Wald Chi² tests).

<table><thead><tr><th></th><th>Chi²</th><th>Df</th><th>p-value<fnref n="1" /></th></tr></thead><tbody><tr><td>Temperature</td><td>38.19</td><td>3</td><td>&lt;0.001 ***</td></tr><tr><td>Light</td><td>9.11</td><td>1</td><td>0.003 **</td></tr><tr><td>Temperature x Light</td><td>9.88</td><td>3</td><td>0.012 *</td></tr></tbody></table>

<figure><img src="image_6.png" /><figcaption>**Fig. 3.** Median abundance of *Curtuteria arguinae* cercariae emerged from *Bittium reticulatum* over 24-h periods in both light and darkness, across five water temperatures. The bars indicate the first and third quartiles.</figcaption></figure>

<footnote n="1">¹ *p* < 0.05; **p* < 0.01; ***p* < 0.001. Df = Degree of freedom.</footnote>
<caption>**Table 3**</caption>

Pairwise comparisons (post-hoc tests: estimated marginal means with Tukey adjustment) of the *Curtuteria arguinae* cercariae abundance at the different temperature and light conditions.

<table><thead><tr><th>Light/Temperature condition</th><th>Pairwise comparison</th><th>p-value<sup>1</sup></th></tr></thead><tbody><tr><td rowspan="6">Light and Dark combined</td><td>18–21 °C</td><td>0.005 **</td></tr><tr><td>18–24 °C</td><td>&lt;0.001 ***</td></tr><tr><td>18–27 °C</td><td>&lt;0.001 ***</td></tr><tr><td>21–24 °C</td><td>0.186</td></tr><tr><td>21–27 °C</td><td>0.001 **</td></tr><tr><td>24–27 °C</td><td>0.357</td></tr><tr><td>18 °C</td><td>Light vs. Dark</td><td>0.011 *</td></tr><tr><td>21 °C</td><td></td><td>0.004 **</td></tr><tr><td>24 °C</td><td></td><td>0.869</td></tr><tr><td>27 °C</td><td></td><td>0.867</td></tr></tbody></table>

### cercariae (8 vs. 12).

To statistically assess the effects of temperature and light conditions on cercariae abundance, a GLMM was performed, excluding the snails #6 and #12 and data at 15 °C (see Materials and Methods). A strong positive effect of temperature ($\chi^2 = 39.19$, p < 0.001) and a more moderate positive effect of light ($\chi^2 = 9.11$, p = 0.0025) (Table 2) were noticed. An interaction between temperature and light was also observed ($\chi^2 = 9.88$, p = 0.0197), suggesting that the impact of light conditions depended on the temperature (Table 1). Post-hoc tests revealed that the cercarial output at 18 °C was significantly different from higher temperatures, i.e. 21 °C, 24 °C and 27 °C (p < 0.05) (Table 3), and between temperatures 21 °C and 27 °C (p = 0.0014). Post-hoc tests showed a significant difference between light and dark conditions at 18 °C and 21 °C (p < 0.05) but not at 24 °C or 27 °C. This indicates that light conditions stimulated cercarial emergence only at moderate temperatures (18 °C and 21 °C), with more cercariae emerging in light. At higher temperatures (24 °C and 27 °C), however, a relatively high number of cercariae emerged under both light and dark conditions (Table 3 and Fig. 3).

## 3.2. Field monitoring of cockle infection

Pooling data from the 22-year database, which included 4,586 dissected cockles, the number of *C. arguinae* metacercariae per cockle was analyzed in relation to cockle shell length (Fig. 4). The shell length of the sampled cockles ranged from 1 to 39 mm, with more than 40 individuals dissected for each 1-mm size class. Infection began at a shell length of 2 mm and progressively increased with cockle size, reaching an average of more than 20 metacercariae per cockle for those larger than 30 mm. However, parasite intensity in individual cockles could be as high as 848 metacercariae (not shown).

Out of 22 years, ten cockle cohorts infected by *C. arguinae* were identified and examined in relation to sea and air temperatures and cockle shell length to assess the factors influencing the first infection of a cockle cohort (Fig. 5 and Table 4). The first infection of cockles by *C. arguinae* metacercariae occurred relatively late in the summer, never before the end of July, and most often during the second half of August. On average, first infection occurred on August 22 with a mean sea temperature of 20.8 °C. The lowest sea temperature recorded for infection was 19.6 °C (in 2007). However, reaching such a temperature alone did not trigger infection. Several cockle cohorts experienced sea temperatures of at least 20 °C in July (e.g., in 1999, 2007, 2009, 2011 and 2014) without infection, which occurred a month later (Fig. 5A). Conversely, the cohorts exposed to sea temperatures of 21.4 °C or higher during their first summer (with a maximum of 22.3 °C in July 2003) were all infected by *C. arguinae*. The lowest air temperature associated with infection was 23.1 °C (in 2002). However, similar to sea temperature, reaching 23 °C did not guarantee infection. Several cohorts encountered this air temperature in June or July without infection, which was delayed by one or two months (Fig. 5B). However, cohorts exposed to air temperatures of 26.3 °C or higher during their first summer (with a maximum of 28.4 °C in July 2003) were all infected. Finally, our results suggest that cockle shell length has a minimal effect on the timing of the first *C. arguinae* infection (Fig. 5C). For example, the first infection occurred in cockles with shell lengths of 5.6 mm in August 2008, compared to 19 mm in August 2007, with other years showing

<figure><img src="image_7.png" /><figcaption>**Fig. 4.** Mean abundance of *Curtuteria arguinae* metacercariae per cockle (white bars) and sampling effort (dotted line) according to cockle shell length.</figcaption></figure>

<footnote n="1">¹ * p < 0.05; **p < 0.01; ***p < 0.001.</footnote>
<figure><img src="image_8.png" /><figcaption>**Fig. 5.** Mean sea temperature (A), maximum daily air temperature (B), and mean cockle shell length (C) in relation to the probable date of first infection by *Curtuteria arguinae* (see Materials and Methods) over the 10 years (out of 22 studied) when cockles recruited and were infected by *C. arguinae*. The estimated date of first infection of each cockle cohort is marked by a larger symbol with the corresponding year.</figcaption></figure>
<table><caption>**Table 4**
Estimated dates of first infection of newly recruited cockle (*Cerastoderma edule*) cohorts by *Curtuteria arguinae*, along with corresponding mean cockle shell length, mean sea temperature and maximum daily air temperature.</caption><thead><tr><th>Cockle cohort</th><th>Date of first infection</th><th>Mean sea temperature (°C)</th><th>Maximum daily air temperature (°C)</th><th>Cockle shell length (mm)</th></tr></thead><tbody><tr><td>1998</td><td>July 25</td><td>19.7</td><td>24.8</td><td>16.5</td></tr><tr><td>1999</td><td>August 23</td><td>22.2</td><td>26.3</td><td>17.5</td></tr><tr><td>2002</td><td>August 26</td><td>20.1</td><td>23.1</td><td>10.0</td></tr><tr><td>2003</td><td>July 30</td><td>22.3</td><td>28.4</td><td>13.9</td></tr><tr><td>2007</td><td>August 22</td><td>19.6</td><td>24.6</td><td>19.3</td></tr><tr><td>2008</td><td>August 18</td><td>21.4</td><td>24.9</td><td>5.6</td></tr><tr><td>2009</td><td>August 30</td><td>19.7</td><td>25.2</td><td>15.7</td></tr><tr><td>2011</td><td>August 30</td><td>21.5</td><td>25.7</td><td>12.7</td></tr><tr><td>2012</td><td>July 27</td><td>20.7</td><td>26.3</td><td>12.0</td></tr><tr><td>2014</td><td>August 21</td><td>20.8</td><td>25.7</td><td>6.9</td></tr></tbody></table>

intermediate shell lengths.

## 4. Discussion

The experimental emergence of cercariae from needle snails and the monitoring of cockle infections by *Curtuteria arguinae* support the conclusion that transmission from the first to the second intermediate host occurs in relatively high water temperature, which coincides with a late summer infection.

The prevalence in the field (<1.6 %), calculated from the number of snails releasing cercariae, likely underestimates the actual prevalence of infected snails due to the presence of infected individuals that do not release cercariae (Born-Torrijos et al., 2014; Curtis and Hubbard, 1990). Nevertheless, the observed prevalence is low but remains consistent with levels typically reported for first intermediate hosts of various trematode species (Thieltges et al., 2008), including the closely related species *C. australis* (3.2 %, Allison, 1979). The emergence rate of *C. arguinae* from *Bittium reticulatum*, when combining values from light and dark conditions, fluctuated greatly among needle snails, as has been observed in many other trematode species (Lo and Lee, 1996; Toledo et al., 1999). Indeed, conspecific trematode clones may exhibit varying levels of phenotypic variability, including emergence traits, such as cercarial output and activity in response to temperature and morphological, behavioural and survival features of emerged cercariae. Although these differences may vary over time (Berkhout et al., 2014; Koehler et al., 2011). Nonetheless, temperature had a significant effect on cercarial emergence, with infected snails releasing significantly more cercariae as of 21 °C, following an increasing trend. Median emergence rates within this temperature range (12–47 cercariae.day⁻¹) were of the same order of magnitude as those of *C. australis* (Allison, 1979), but low compared to other echinostomatid species. For example, daily cercarial outputs of 147–708 cercariae were reported for *Himasthla elongata*, 89 for *H. continua*, 320 for *H. rhigedana*, and more than 2000 for *H. quissetensis* (de Montaudouin et al., 2016; Prokofiev et al., 2016; Thieltges et al., 2008). It is often observed that the cercarial production is inversely related to cercariae size, with smaller cercariae being produced in greater numbers than larger ones (Loker, 1983). However, this general relationship does not explain the low emergence rate observed for *C. arguinae*, whose cercariae are actually smaller, measuring approximately 300 µm in length (Stout et al., 2025), than those of the previously mentioned species, which range from 500 to 644 µm in length (Adams and Martin, 1963; Allison, 1979; Galaktionov et al., 2021; Loos-Frank, 1967; Stunkard, 1938).

Many factors may trigger cercarial emergence from their first intermediate hosts (Studer and Poulin, 2013), and the importance of these factors is species-specific. While salinity and light can act as a simulating factors (Bommarito et al., 2020; Mouritsen, 2002b; Prokofiev et al., 2023; Soldánová et al., 2022), water temperature was reported as the primary factor influencing cercarial emergence (positively or

negatively), while other factors are generally ranked lower in the hierarchy of environmental cues (Fingerut et al., 2003; Schmidt and Fried, 1996). This aligns with our findings, which suggest that a temperature threshold required to significantly stimulate cercarial release of *C. arguinae* lies somewhere between 18 °C and 21 °C. The highest emergence rate was observed at 27 °C (our highest temperature tested), where daily outputs were maximal regardless of light conditions. Light conditions also influenced cercarial outputs, but to a lesser extent. Light interacted with temperature under moderately warm conditions (18 °C and 21 °C), with lower emergence in dark conditions at 18 °C and 21 °C, but no significant difference between light and dark at 24 °C or 27 °C. Similar interactions between environmental factors influencing emergence have been observed in previous studies (Mouritsen, 2002b; Shostak and Esch, 1990; Studer and Poulin, 2013). The thermal window for cercarial emergence is highly species-specific but generally ranges between 15 °C and 25 °C, with colder temperatures typically coinciding with higher latitudes (Fingerut et al., 2003; Morley and Lewis, 2013; Prokofiev et al., 2016, 2023).

This study shows that optimal cercarial emergence for *C. arguinae* occurs in light and relatively warm environmental conditions. Nonetheless, it is plausible that temperature does not directly influence cercarial emergence but rather affects the activity of its first intermediate host, and that this change of activity acts as a signal for cercariae to emerge. In terms of adaptive evolution, it may be more probable that the parasite detects optimal conditions for cercarial emergence by aligning with a single factor variation (such as host activity), rather than responding to multiple factors that require various stimuli receptors (Mouritsen, 2002a). Another argument minimizing the direct effect of the temperature on parasite emergence is that, in mid-latitudes, the minimum development threshold temperature (MDTT) is evaluated as equal or below 10 °C while the minimum emergence threshold temperature (METT) ranges from 7 to 14 °C (Morley and Lewis, 2013). This suggests that maturation and release of cercariae would be possible for most of the year in Arcachon Bay, which is not the case according to downstream host (cockle) infection. Additionally, our field monitoring indicated that temperature alone did not explain cockle infection by *C. arguinae*, even though summer infections were typical, as seen in the New Zealand species *C. australis*, which has an emergence rate that peaks at 25 °C (Allison, 1979). The interannual variability in the start of infection, which coincides with cercarial emergence, spans over a month in our study and may correspond to a 2 °C difference in sea temperature and a 5 °C difference in maximum air temperature, which is significant in intertidal habitats. Apart from temperature, cercariae were able to infect cockles with a wide range of shell lengths, even small individuals (e.g. 2 mm), as commonly observed in other echinostomatid species (de Montaudouin et al., 2005; Jensen et al., 1999), meaning that the first infection of the parasite’s second intermediate host does not seem to be dependant of its size.

This preliminary investigation requires deeper insight to fully understand the phenology of these parasite-hosts interactions. At this stage, a scenario can be proposed for the specific system on Banc d'Arguin (Arcachon Bay, France), bearing in mind that the primary objective for the parasite is to infect its downstream host (Prokofiev et al., 2016). During spring, the intertidal *Zostera noltii* meadow grows, and populations of *B. reticulatum* are settling in vegetated intertidal pools, which are suitable habitats for needle snails (Arroyo et al., 2006; Do et al., 2011), but also, are considered hotspots for trematode infection (Thieltges and Rick, 2006). These snails actively graze on epiphytes, along leaves, and might become infected by miracidia released from oystercatcher feces and floating in the water during tidal flow (Stout et al., 2025). In late summer, under warm and light conditions, needle snails are most active and optimally disperse the parasite’s cercariae (Mouritsen, 2002a), which have only a few hours to infect cockles (Allison, 1979). While there is no evidence that these parasites manipulate their second intermediate hosts, they are suspected of contributing to host mortality (Desclaux et al., 2006).
<figure><img src="image_9.png" /><figcaption>**Fig. 6.** Known distribution of *Curtuteria arguinae* (in cockles) and of its main hosts along the northeastern Atlantic coast (excluding the Mediterranean and Baltic Seas): *Bittium reticulatum* (first intermediate host), *Cerastoderma edule* (second intermediate host) and *Haematopus ostralegus* (definitive host). Footnote: Sources by host species: *B. reticulatum*: Bououarour et al. (2021); Høisæter (2009); Skewes (2008); Smith (2021); Wolff et al. (1993); Jean-Philippe Pezy pers. comm.; *C. edule*: de Montaudouin et al. (2021); Hayward and Ryland (2017); Honkoop et al. (2008); Krakau et al. (2012); Mahony et al. (2020); Símonarson (1981); *H. ostralegus*: Hockey et al. (2020); Lepage (2003); van de Pol et al. (2014).</figcaption></figure>

The current distribution of *C. arguinae* in its second intermediate host, the cockle, spans from Arcachon Bay (44°N, France) to Dakhla (23°N, Morocco) (de Montaudouin et al., 2009), confirming that this species is more adapted to warm climates. There has also been an observation in Brittany (48°N, France), though with a low infection level and an uncertain persistence (de Montaudouin et al., 2009). The expansion of this parasite distribution depends on the distribution of hosts and environmental conditions, particularly sea temperature. Currently, the distribution of the hosts is significantly broader than that

of *C. arguinae* (Fig. 6). The definitive host, the European oystercatcher (*Haematopus ostralegus*), can breed as far north as northern Norway (70°N) and winters as far south as Ghana (4°N) (van de Pol et al., 2014). The distributions of the first and second intermediate hosts (*B. reticulatum* and *C. edule*, respectively) extend from northern Norway and Murmansk, Russia, (69°N) to Mauritania (19°N) and Senegal (14°N), respectively (Hayward and Ryland, 2017; Høisæter, 2009; Krakau et al., 2012; Wolff et al., 1993). However, *B. reticulatum* appears to be discontinuously distributed along the northern European coastline,
absent from part of the northern French coast (eastern English Channel) and the North Sea further south than Orkney, UK and Limfjord, Denmark (Smith, 2021). Regarding the parasite, the lack of data on trematodes in cockles prevents any conclusion about the presence of *C. arguinae* further south, near Dakhla, Morocco. In contrast, there is extensive literature to support that *C. arguinae* is still absent or rare north of 44°N (de Montaudouin et al., 2009, 2021; Mahony et al., 2022; Thieltgès et al., 2013). Though a few metacercariae in cockles were reported once in Brittany, France (48°N) (de Montaudouin et al., 2009), this isolated record suggests possible presence but does not confirm a stable, established population.

In general, *C. arguinae* could potentially expand northward into regions where all hosts are present, from northern France to Scandinavia excluding the southern North Sea, where one host species remains unrecorded for the moment (Fig. 6). Yet current summer temperatures in these areas may be too low to allow effective transmission. Indeed, the parasite's northern range limit seems to be determined by temperature, which influences both the emergence of the cercariae but also the distribution of the first intermediate host itself. This gastropod is particularly abundant and widespread in more temperate regions such as the Mediterranean Sea or southern parts of the Northeast Atlantic (Smith, 2021). While it tolerates colder conditions further north, its populations there tend to be smaller and more patchily distributed, suggesting a preference for warmer environments.

However, surface ocean temperatures in the North Atlantic Ocean are expected to increase, with an average rise of +2.1 °C by 2100 (with 90 % confidence interval ranging from 0.6 to 4.7 °C, referred to as of Sea Surface Temperatures), under the high emissions scenario (EEA; 2025). These trends could be more pronounced in shallow waters where needle snails are the most abundant. This could lead to population increases and a broader distribution of the snail in northern regions. Simultaneously, *C. arguinae* could encounter more favorable summer temperatures, enhancing cercarial output and improving transmission efficiency to successfully infect cockles.

At the same time, warming is also likely to influence *C. arguinae* infections in the southern parts of its current range. Elevated temperatures could increase cercarial emergence, and although cercarial survival may be reduced, transmission success and subsequent infection intensity in the second intermediate host—the cockle—might rise, as suggested by Studer et al. (2010). As *C. arguinae* is suspected to induce mortality in its second intermediate host (Desclaux et al., 2006), warmer conditions could ultimately increase the risk of parasite virulence and cockle mortality through increased parasite-induced deleterious behavioural changes or morphological impacts, making cockles more susceptible to further infections, environmental stress and predation. A comparable scenario has been reported in Denmark, where mass mortality of the crustacean second intermediate host of a microphallid trematode followed unusually warm conditions that boosted cercarial output and subsequent infections (Jensen and Mouritsen, 1992). These dynamics may extend beyond individual hosts, potentially resulting in impacts at both population and ecosystem levels, given the cockle's ecological importance as an engineer species shaping benthic communities. On the other hand, climate change may contribute to habitat losses. For instance, seagrass meadows, which are one of the preferred habitats of *B. reticulatum*, are at moderate risk at 1.5 °C global warming, but face a significantly higher risk of severe impacts, with a high probability of irreversibility, if warming exceeds 2 °C (IPCC, 2019). One of the snail's preferred habitat might thus experience a decline, which would have the opposite, negative effect on total cercarial load and cockle infection intensity.

In conclusion, the relatively widespread distribution of all hosts necessary for completing the life cycle of *C. arguinae*, and their potential to broaden their range, make it likely that this parasite will spread into cockle populations of northern France and northern Europe, potentially affecting their population dynamics. The extent of this propagation will depend on the effects of climate change, particularly on the balance

between the positive impact of rising temperatures on parasite transmission and the negative impact on seagrass health, a key habitat for the first intermediate host *B. reticulatum*. Ultimately, the fate of the definitive host populations may also play a role. European oystercatcher population are declining in the Netherlands, Germany, and Denmark, with the causes remaining largely unknown (van de Pol et al., 2014). Future research is needed to better understand the phenology of *C. arguinae*, especially regarding transmission between the definitive and first intermediate hosts. There are indications that, in certain zonotic areas, almost half of the European oystercatcher population may be infected with *C. arguinae* (Stout et al., 2025), but the transmission process to the first intermediate host and the development of miracidia within it remain poorly understood.

### CRediT authorship contribution statement

**Leslie Stout:** Writing – review & editing, Writing – original draft, Visualization, Validation, Methodology, Formal analysis, Data curation, Conceptualization. **Itsaso Lopez-Ahedo:** Formal analysis. **Guillemine Daffe:** Writing – review & editing, Project administration. **Aurélie Chambouvet:** Writing – review & editing, Project administration. **Xavier de Montaudouin:** Writing – review & editing, Writing – original draft, Validation, Supervision, Resources, Project administration, Methodology, Investigation, Formal analysis, Conceptualization.

### Funding sources

This work is part of Leslie Stout's doctoral thesis (University of Bordeaux – 2022-RJ-114) financed by a doctoral grant of the French Ministry for Higher Education and Research. Part of this project was funded by the INTERREG-ATLANTIC program through the research project COCKLES (EAPA_458/2016 COCKLES Co-Operation for Restoring CocKle SheLlfisheries & its Ecosystem-Services in the Atlantic Area).

### Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

### Acknowledgements

Sampling was carried out with the support of the *Planula* 4 vessel (CNRS-INSU, Flotte Océanographique Française). We also extend our thanks to the staff of SEPANSO Aquitaine, in charge of the management of Banc d'Arguin's National Natural Reserve. Finally, we thank the BenthOBS network for sharing data on *Bittium reticulatum*.

### Data availability

Data will be made available on request.

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