Simão Correia

Luísa Magalhães
email: luisa.magalhaes@ua.pt

Rosa Freitas

Hocein Bazairi

Meriam Gam

Xavier De Montaudouin

Simão a , Magalhães, Luísa Correia

Xavier Montaudouin

Large scale patterns of trematode parasite communities infecting Cerastoderma edule along the Atlantic coast from Portugal to Morocco

Keywords: Formal analysis, Investigation, Writing -Original draft Conceptualization, Methodology, Formal analysis, Investigation, Writing -Review Resources, Supervision. Hocein Bazairi: Conceptualization, Methodology, Investigation, Resources. Meriam Gam: Investigation. Xavier de Montaudouin: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Writing -Review Cockle, Spatial survey, Host-parasite system, Abiotic drivers, Coastal waters, Community composition

In this study, spatial sampling was performed from North Portugal to South Morocco to analyse trematode communities of the widespread bivalve Cerastoderma edule, host of several trematode species. From the twelve trematode species found in this study, nine were present in multiple aquatic systems demonstrating high trematode dispersal ability, driven by the presence of all the hosts. Multivariate analysis related to trematode communities in cockles clustered: 1) Portuguese aquatic systems influenced by cold waters, leading to low trematode abundance; 2) coastal systems characterized by dominance of trematode Parvatrema minutum and muddy sediments; 3) lagoons (or bays) with high oceanic influence and high trematode diversity. These findings suggested that, besides host species presence, temperature is an important trigger for parasite infection, with coastal upwelling operating as a shield against trematode infection in Portugal and masking latitudinal gradients. Results highlighted the possible consequences of thermal modification mediated by oceanographic global circulation change on cockle populations.

Introduction

Coastal aquatic systems are known for their high diversity and importance to populations of migratory and resident species [START_REF] Levin | The function of marine critical transition zones and the importance of sediment biodiversity[END_REF]. These aquatic systems have high economic value providing many natural resources and settlement sites for human population [START_REF] Basset | Estuarine and lagoon biodiversity and their natural goods and services[END_REF]. In these ecosystems, a considerable part of the animal biological diversity are parasitic species, corresponding approximately, to 2/5 of eukaryotic total species richness [START_REF] Dobson | Homage to Linnaeus: How many parasites? How many hosts?[END_REF][START_REF] Hudson | Is a healthy ecosystem one that is rich in parasites?[END_REF]. These parasites are also ubiquitous in every free-living community. However, they remain neglected in most global community analyses. In terms of functional diversity, parasites play a key structuring role in communities, providing information about the ecosystem functioning [START_REF] Hudson | Is a healthy ecosystem one that is rich in parasites?[END_REF][START_REF] Marcogliese | Parasites: Small Players with Crucial Roles in the Ecological Theater[END_REF][START_REF] Dairain | Influence of parasitism on bioturbation: from host to ecosystem functioning[END_REF]. They impose adverse effects on their hosts phenotype and health [START_REF] Marcogliese | Parasites: Small Players with Crucial Roles in the Ecological Theater[END_REF] which may result into high mortality at population scale [START_REF] Curtis | Growth, trematode parasitism, and longevity of a long-lived marine gastropod (Ilyanassa obsoleta)[END_REF]Fredensborg et al., 2005;[START_REF] O'connell-Milne | Reduced growth, body condition and foot length of the bivalve Austrovenus stutchburyi in response to parasite infection[END_REF]. At higher scale, they induce significant impact on environmental functions [START_REF] Thomas | Parasites and Ecosystem Engineering: What Roles Could They Play?[END_REF], exacerbated in a climate change framework (Mouritsen et al. 2005[START_REF] Marcogliese | The impact of climate change on parasites and infectious disease of aquatic animals[END_REF]).

Thus, parasites are considered ecosystem engineers by interfering with the host local population and consequently affecting the value and impact of these species in the ecosystem [START_REF] Thomas | Parasites and Ecosystem Engineering: What Roles Could They Play?[END_REF]. This role is magnified when the host species itself is also an ecosystem engineer [START_REF] Dairain | Influence of parasitism on bioturbation: from host to ecosystem functioning[END_REF].

In coastal waters, including bays, estuaries and coastal lagoons, trematodes are the most abundant and common macroparasites [START_REF] Lauckner | Diseases of mollusca: bivalvia[END_REF][START_REF] Roberts | foundations of parasitology[END_REF]. They have a complex and heteroxenous life cycle, infecting more than one host species to complete their life cycle [START_REF] Bartoli | Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean[END_REF] with alternation between asexual multiplication and sexual reproduction phases [START_REF] Whitfield | Parasitic helminths[END_REF]. The typical trematode life cycle includes a free-living larva (miracidium) that hatches from the egg and infects first intermediate hosts, most of the time a mollusc. At this stage, the parasite transforms into a mother sporocyst that will develop, depending on the trematode species, into a mature sporocyst or into redia. Within the sporocysts or rediae, cercariae free-living stages develop by asexual multiplication. Cercariae will emerge from the first host and reach the second intermediate host, an invertebrate or a vertebrate species depending on the trematode species. The cercariae penetrate the second intermediate host and metamorphose into metacercariae. The cycle is complete when the parasitized second intermediate host is predated by the final host, a vertebrate species. Then, each metacercaria transforms into an adult form that will reproduce sexually and produce eggs [START_REF] Bartoli | Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean[END_REF][START_REF] Esch | The Transmission of Digenetic Trematodes: Style, Elegance, Complexity[END_REF][START_REF] Roberts | foundations of parasitology[END_REF].

The complex life cycle described here, shows not only how important host diversity is in the distribution of trematode parasites, but also highlights that environmental parameters must have a key role in the modulation of parasite population dynamics, especially by their impact on infective free-living larvae transmission and infection success [START_REF] Anderson | Abiotic versus biotic hierarchies in the assembly of parasite populations[END_REF]de Montaudouin et al., 2016ade Montaudouin et al., , 2016b;;[START_REF] Koprivnikar | Effects of temperature, salinity and water level on the emergence of marine cercariae[END_REF]Studer and Poulin, 2013). Indeed, a greater host diversity is usually reflected in a greater diversity of parasites, particularly for those with complex life cycles [START_REF] Sukhdeo | Trematode behaviours and the perceptual worlds of parasites[END_REF] and in the same sense, a higher abundance of suitable hosts increases the abundance and prevalence of parasites in the ecosystem (Combes, 1991). As an example, [START_REF] Hechinger | Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts[END_REF] found a positive correlation between bird communities composition (the final hosts of several trematode species) and trematode communities composition in a snail host.

Similarly, [START_REF] Thieltges | Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve[END_REF] demonstrated higher metacercariae abundance (the trematode parasitic stage occurring in the second intermediate host) positively correlated to an increase in abundance and diversity of the higher trophic level host communities. On the other hand, higher host density can also promote a dilution effect and therefore decrease the parasite burden in a specific host [START_REF] Buck | Host density increases parasite recruitment but decreases host risk in a snailtrematode system[END_REF][START_REF] Magalhães | Cockle population dynamics: recruitment predicts adult biomass, not the inverse[END_REF][START_REF] Mouritsen | Spatial heterogeneity in parasite loads in the New Zealand cockle: The importance of host condition and density[END_REF]. Concerning the abiotic environmental factors, different conditions of temperature (Achiorno and Martolrelli, 2016;de Montaudouin et al., 2016a), salinity and pH [START_REF] Koprivnikar | Effects of temperature, salinity, and pH on the survival and activity of marine cercariae[END_REF][START_REF] Koprivnikar | Effects of temperature and salinity on emergence of Gynaecotyla adunca cercariae from the intertidal gastropod Ilyanassa obsoleta[END_REF][START_REF] Mouritsen | The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity[END_REF]Studer and Poulin, 2013), among others, can also have an influence on trematode dynamics [START_REF] Wilson | Heterogeneities in macroparasite infections: patterns and processes[END_REF]. As an example, a higher cercariae emission from the first intermediate host is related to an increase on the water temperature (de Montaudouin et al., 2016a) and consequently a higher trematode infectivity [START_REF] Thieltges | Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae)[END_REF]. Favourable salinity conditions have been reported to benefit, as well, trematode emergence from the first intermediate host [START_REF] Koprivnikar | Effects of temperature and salinity on emergence of Gynaecotyla adunca cercariae from the intertidal gastropod Ilyanassa obsoleta[END_REF][START_REF] Lei | Effects of salinity on multiplication and transmission of an intertidal trematode parasite[END_REF].

Bivalves (along with several other molluscs) are suitable and frequent first and/or second intermediate hosts for trematode parasites [START_REF] Lauckner | Diseases of mollusca: bivalvia[END_REF], especially because they are easily invaded by trematodes free-living stages through their suspension-feeding activity. Cerastoderma edule, the edible cockle, is among the most common and widely distributed bivalve species of the northeast Atlantic coast, from Norway [START_REF] Dabouineau | Synthesis on biology of Common European Cockle Cerastoderma edule[END_REF] to Mauritania [START_REF] Honkoop | Molluscan assemblages of seagrass-covered and bare intertidal flats on the Banc d'Arguin, Mauritania, in relation to characteristics of sediment and organic matter[END_REF]. Cockles are extensively commercially exploited presenting therefore high socio-economic value. Besides, cockles display a crucial ecological role, linking primary producers to higher trophic levels (key species) and acting as ecosystem engineer [START_REF] Ciutat | Influence of cockle Cerastoderma edule bioturbation and tidal-current cycles on resuspension of sediment and polycyclic aromatic hydrocarbons[END_REF][START_REF] Morgan | Climate change impacts on potential recruitment in an ecosystem engineer[END_REF][START_REF] Rakotomalala | Modelling the effect of Cerastoderma edule bioturbation on microphytobenthos resuspension towards the planktonic food web of estuarine ecosystem[END_REF]. This bivalve species acts as first and/ or second intermediate host of several trematode species [START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF][START_REF] Longshaw | A review of the infectious agents, parasites, pathogens and commensals of European cockles (Cerastoderma edule and C. glaucum)[END_REF] and, when compared to other bivalves, parasitic communities of cockles are particularly diverse and abundant. For these reasons, cockles and their associated trematode fauna are a good model to study host/parasite interactions (e.g. [START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF][START_REF] Lauckner | Diseases of mollusca: bivalvia[END_REF]Thieltges et al., 2006).

The often so called Latitudinal Diversity Gradient, describing that species richness increases from the poles to the tropics, is a pattern widely recognized and applicable to many terrestrial and marine species [START_REF] Hillebrand | On the Generality of the Latitudinal Diversity Gradient[END_REF]. However, the causes that determine this gradient are not yet fully understood, with hypotheses that go from higher migration rates to the tropics [START_REF] Jablonski | Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient[END_REF] and/ or a lower climate variation that allows the accumulation of species [START_REF] Guo | Species richness in plant genera disjunct between temperate eastern Asia and North America[END_REF], to the greater opportunity of species to specialize due to the high productivity and environmental stability, characteristic of tropical habitats [START_REF] Harrison | Toward a better understanding of the regional causes of local community richness[END_REF][START_REF] Mittelbach | Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography[END_REF]. Nonetheless, when referring to parasitic species, the knowledge is more limited and the observation of latitudinal patterns, especially in the case of parasites with complex life cycles, it is not so evident [START_REF] Poulin | Latitudinal gradient in the taxonomic composition of parasite communities[END_REF][START_REF] Stephens | The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts[END_REF]. Despite the recent study efforts on latitudinal patterns of parasites [START_REF] Poulin | Parasite biodiversity[END_REF]Studer et al., 2013;[START_REF] Thieltges | Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe[END_REF][START_REF] Thieltges | Host diversity and latitude drive trematode diversity patterns in the European freshwater fauna[END_REF][START_REF] Torchin | Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts[END_REF], results are usually conflicting. For instance, [START_REF] Rohde | Latitudinal differences in species and community richness and in community structure of metazoan endo-and ectoparasites of marine teleost fish[END_REF] observed an increase in the diversity and abundance of monogenean parasites towards the tropics, however, in the same study, no latitudinal gradient was observed for digenean parasites. Studer et al. (2013) have not found evidences of latitudinal patterns when working with the cockle Austrovenus stutchburyi and trematodes as host-parasite model, while [START_REF] Mouritsen | Spatial heterogeneity in parasite loads in the New Zealand cockle: The importance of host condition and density[END_REF] have demonstrated an increase of trematode diversity in a snail intermediate host at higher latitudes. An opposite pattern was observed by [START_REF] Thieltges | Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe[END_REF] for trematode communities infecting a crustacean host.

The present study aimed to provide, for the first time, a large spatial survey of trematode communities infecting Cerastoderma edule in the southern range of its distribution area, i.e. from the North of Portugal to the South of Morocco. The tested hypotheses were: 1) trematode communities follow a latitudinal gradient driven by abiotic latitudinal-related factors and 2) trematode communities abundance and/ or diversity is dependent on the type of studied system (lagoon vs. estuary vs. bay).

Material and Methods

Study Area

The present study was conducted in a total of seventeen semi-diurnal tidal marine systems distributed along Portugal and Morocco coastline (Figure 1 Through literature review, information on annual variation of water temperature and salinity for each sampled aquatic system at each respective sampled year (whenever possible) was obtained and gathered in Table 1.

Throughout this manuscript, the term 'coastal lagoon' is used when referring to coastal water bodies, connected to the ocean through one or more inlets and separated by a barrier. The lagoons vary from oligohaline to hypersaline conditions [START_REF] Gooch | Challenges in the Policy-Environment-Modelling management context (Chapter 01)[END_REF]. 'Estuaries' were considered as semi-enclosed coastal water bodies, that have a connection with the open sea and within which seawater is measurably diluted with fresh water derived from land drainage [START_REF] Pritchard | What Is an Estuary: Physical Viewpoint[END_REF]. When in the presence of large bodies of water that enters through the coast and are intimately connected to an ocean by a wide entrance, the term 'bay' was used (UN, 1982).

Field sampling and parasite identification

At each sampling area, sediment samples were collected to perform grain size analysis following the method described by [START_REF] Quintino | Assessment of macrozoobenthic communities in the lagoon of Óbidos, western coast of Portugal[END_REF]. Silt and clay fraction (fine particles with diameter below 63 µm) were assessed by wet sieving and the remaining fractions (sand and gravel) were determined by sieving through a column of five sieves with decreasing mesh sizes (2.00, 1.00, 0.50, 0.250 and 0.125 mm).

Cockles were collected in the intertidal zone (with exception of Óbidos lagoon) using six quadrats (0.25 m 2 each) randomly placed along a 100 m parallel to the water transect and by sieving the sediment through a 1-mm mesh. The number of cockles per square meter (density) was then estimated. In the Óbidos lagoon, a subtidal area where the quadrat method was impossible to perform, samples were collected with a hand dredge and cockle density (d) was calculated following the equation:

. = × ×
where "n" corresponds to the total number of cockles collected; "a" to the hand dredge area (m 2 ); "t" the mean number of trawls (mean number of times the dredge was dragged in the sediment per launch); and "I" the total number of launches.

Shell length (SL) of each cockle was measured to the lowest mm with a calliper.

From each aquatic system, according to availability, a variable number (between 11 and 65) of adult cockles (23 -30 mm) were dissected. In Albufeira lagoon and Mira estuary, due to low abundance of cockles from this length class, twenty cockles representing the SL of each area (16 -31 mm and 8 -18 mm, respectively) were dissected. Cockle flesh was squeezed between two glass slides and observed under a stereomicroscope. All trematodes were identified to the species level following de [START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF] identification key.

Parasite abundance (mean number of trematode metacercariae per cockle), prevalence (percentage of infected cockles by trematode species) and trematode species richness (number of trematode species present) were calculated according to [START_REF] Bush | Parasitology Meets Ecology on Its Own Terms: Margolis et al. Revisited[END_REF].

Data analysis

To test the influence of latitude (independent variable) on the variation of trematode species richness (TSR), trematode total prevalence (TTP) and trematode mean abundance (TMA) (dependent variables), individual regression analyses were performed using the SPSS v.25 software.

The Chbika estuary, due to the lack of abiotic information, was excluded from all the following multivariate analyses and used only on trematodes descriptive information.

The data matrix with the abundance of trematode per site [abundance per trematode species metacercariae x sampling site] was square root transformed and the Bray-Curtis [START_REF] Legendre | Numerical ecology[END_REF] similarity calculated between sites. To identify the biological affinity groups, the resemblance matrix was then analysed using a hierarchical clustering analysis tool. The affinity groups were characterized according to environmental and biological features by calculating the mean value of annual maximum and minimum water temperature, annual maximum and minimum water salinity, median grain-size, cockle density at sampling time and by calculating the rarefaction index, i.e. an estimation of the trematode species diversity through standardization of the number of samples [START_REF] Gotelli | Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness[END_REF]. Differences in terms of trematode metacercariae abundance were then tested among affinity groups, type of aquatic system (lagoons vs estuaries) and geographical position (north vs. south of strait of Gibraltar). Differences were tested using permutational multivariate analysis of variance [START_REF] Anderson | PERMANOVA + for PRIMER: guide to software and statistical methods[END_REF] following unrestricted permutation of the raw data (9999 permutations) and the calculation of type III sums of squares. Similarity Percentages (SIMPER) were used to characterize the type of aquatic system and the geographical position by the species that most contributed to the dissimilarity between groups. Affinity groups differences were visualized through Principal

Coordinates Ordination analysis (PCO) after a distance among centroids resemblance [START_REF] Clarke | Change in Marine Communities: An approach to statistical analysis and interpretation[END_REF]. The abiotic variables that were highly correlated (Spearman ρ > |0.7|) to samples ordination were represented as superimposed vectors in the PCO graph.

To model the relationship and provide quantitative measures of abiotic and biotic data (annual maximum and minimum water temperature, annual maximum and minimum water salinity and median grain-size and cockle density) on metacercariae community of each aquatic system, a Distance-based linear model (DistLM) was performed [START_REF] Anderson | PERMANOVA + for PRIMER: guide to software and statistical methods[END_REF]. The results were obtained using appropriate permutation (9999 permutations) and following the step-wise method and Akaike information criterion (AICc). This criterion balances between data fitness and the most parsimonious model (the model with lower power loss). Thus, it is considered the best model, among the possible ones, the one showing the lowest AIC [START_REF] Symonds | A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion[END_REF]. Distances among aquatic systems were visualized through a dbRDA plot.

All multivariate analyses were performed using the PRIMER v.6 software. 3).

Results

Trematode species richness, prevalence and abundance

Overall, trematode species richness (TSR, considering all identified trematode species) increased linearly from north to south but accounting for only 22% of the total variation (R 2 = 0.22). When excluding Chbika and Sebou, two small estuaries that displayed the lowest species richness in this study (1 trematode species each), the linear model fitted better with latitude, explaining 61% of total variation (Table 3).

Trematode total prevalence (TTP, considering all identified trematode species)

decreased with the latitude as demonstrated by the quadratic equation that explained 82% of the TTP variety (R 2 = 0.82; Table 3). The Óbidos lagoon (39 °N, Portugal) showed the lowest TTP value (6%) whereas, almost every aquatic system south of 36 °N presented 100% of TTP (except Loukkos estuary, 35 °N) (Table 4).

Trematode mean abundance (TMA, considering trematode species infecting cockles as second intermediate host) did not follow significantly any model. Nonetheless, a higher TMA was observed in the central zone of the total extent of the sampled area in comparison to the aquatic systems located at the northern and southern edges of the total area sampled in this study. The Óbidos lagoon (39 °N, Portugal) presented the lowest TMA (0.03 ± 0.17 metacercariae.cockle -1 ) whereas, Oum Er Rbia (33 °N, Morocco) presented the highest TMA (820 ± 595 metacercariae.cockle -1 ).

Multivariate analysis

Cluster analysis, at a similarity distance of 70%, allowed to assemble the different areas in three affinity groups (Figure 4A and the lowest for groups B1 and B2.2, respectively (Table 5).

The obtained affinity groups were represented on the PCO ordination graph (Figure 4B). The axis 1 of the PCO explained 59% of the total variation, separating the group A which is composed by the majority of the aquatic systems south of 36 °N and classified as estuaries (positive side of the axis) from the group B2 (negative side of the axis), that comprises all aquatic systems north of 36 °N, considered as costal lagoons, and the southernmost sampled aquatic system (Dakhla bay, 23 °N). PERMANOVA results confirmed a significant difference between sites located North and South from the Gibraltar strait (PERMANOVA: 240.37, p < 0.001) mostly driven by the presence of P. minutum and H. quissetensis (Table 6) and a significant difference between estuaries and coastal lagoons (PERMANOVA: 38.94, p < 0.001) particularly dependent also on P. minutum and H. quissetensis (Table 6). Minimum water temperature and cockle density presented a positive correlation to this axis and sediment median grain-size a negative correlation. In turn, axis 2 described 27% of total variation dividing group B2.2 and group A, both in the positive side of the axis, from group B1 in the negative side of the axis. The geographical position (north vs.

south) in relation to the strait of Gibraltar (36 °N) showed again an important effect on these groups separation that was also driven by cockle density (negative correlation).

The best model obtained through the DistLM analysis included the variables sediment median grain-size and cockle density as predictors of trematode community composition, explaining 42 % of the total variation (R 2 = 0.42). When transposed to the dbRDA plot, axis 1 (representing 29 % of total variation), led by the differences in terms of median grain size, separated the aquatic systems north of the strait of Gibraltar (Portuguese aquatic systems) from the southern (Moroccan) aquatic systems with the exception of Sidi Moussa coastal lagoon and Merja Zerga estuary. Axis 2 (explaining 13 % of total variation) was positively correlated to cockle density separating two coastal lagoons of Morocco (Sidi Moussa and Oualidia coastal lagoons) and Oum Er Rbia estuary from the other aquatic systems (Figure 5).

Discussion

Trematode parasites can have a significant impact on population dynamics of their hosts, implying modification on host growth (Wegeberg and Jensen, 2003) or inducing higher mortalities rates [START_REF] Desclaux | Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis[END_REF], which highlights the importance to study host-parasite interactions. This study is among the few reports on large-scale trematode communities infecting cockles (e.g. de [START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF][START_REF] Magalhães | Review: Bucephalus minimus, a deleterious trematode parasite of cockles Cerastoderma spp[END_REF] and represents the first large-scale assessment of latitudinal gradient (and abiotic related factors) as a driver of trematode communities composition in Cerastoderma edule as a host model. In addition, this is the first exhaustive study on trematode species composition in Moroccan cockles.

There are sixteen trematode species infecting Cerastoderma edule in its distributional range that use this bivalve as first and/ or second intermediate host [START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF]. In the present study, a total of 12 species were identified along the whole sampled latitudinal gradient. Nine (Bucephalus minimus, Curtuteria arguinae, Diphterostomum brusinae, Gymnophallus choledochus, Himasthla continua, H. interrupta, H.

quissetensis, Psilostomum brevicolle and Parvatrema minutum) showed a great dispersal ability, since they were present in a wide range, i.e. along the sampled latitudes, possibly related to migration of birds and fish which are trematode final hosts [START_REF] Feis | The most vagile host as the main determinant of population connectivity in marine macroparasites[END_REF]. For a trematode species, to complete its life cycle, the three intermediate/final host species should be present in the same aquatic system [START_REF] Bustnes | Anthropogenic influences on the infestation of intertidal gastropods by seabird trematode larvae on the southern Barents Sea coast[END_REF]. Nonetheless, biogeographical barriers, such as oceans in the case of continental species, are among the most important factors contributing to isolation and prevention of species exchange among regions [START_REF] Cox | Biogeography: An Ecological and Evolutionary Approach[END_REF][START_REF] Ricklefs | Species diversity: regional and historical influences[END_REF].

In the present study, the strait of Gibraltar (36 °N), a known geographical barrier, showed some influence on trematode communities, dividing the observed trematode species in three different categories. [START_REF] Pizzolla | Tritia reticulata Netted dog whelk[END_REF]. Thirdly, H. elongata and Renicola roscovitus displayed a Northern distribution likewise their first intermediate host Littorina littorea, a marine gastropod that inhabits the intertidal zone from the White Sea to Gibraltar, on the Atlantic east coast [START_REF] Johannesson | The paradox of Rockall why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)?[END_REF]. Thus, this study confirms that at this latitudinal scale, the distribution of the trematode species is mainly driven by the occurrence of the first intermediate host [START_REF] De Montaudouin | Distribution of parasites in their second intermediate host, the cockle Cerastoderma edule: Community heterogeneity and spatial scale[END_REF][START_REF] Thieltges | Habitat and transmission -effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve[END_REF][START_REF] Thieltges | Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe[END_REF], considering that final hosts have generally a wider distribution area [START_REF] Magalhães | Review: Bucephalus minimus, a deleterious trematode parasite of cockles Cerastoderma spp[END_REF].

Trematode species richness (TSR) and trematode total prevalence (TTP) increased towards south (from 40 °N to 23 °N). This latitudinal dependent pattern of TSR follows the same trend described for benthic macrofaunal diversity which show higher values with decreasing latitudes [START_REF] Macpherson | Large-scale species-richness gradients in the Atlantic Ocean[END_REF][START_REF] Martins | Diversity, distribution and ecology of the family Syllidae (Annelida) in the Portuguese coast (Western Iberian Peninsula)[END_REF][START_REF] Roy | Beyond Species Richness: Biogeographic Patterns and Biodiversity Dynamics Using Other Metrics of Diversity[END_REF]. However, this pattern was not observed in the case of Chbika and Sebou estuaries, located at 28 °N and 34 °N, respectively, that presented the lowest TSR.

Chbika is not a permanent estuary ('Oued'), which might induce lower macrofaunal and parasite diversity. Conversely, the Sebou river is one of the biggest North African rivers, crossing several riverside populations and then impacted by several anthropogenic activities, including agricultural activities [START_REF] Perrin | Water quality assessment of highly polluted rivers in a semi-arid Mediterranean zone Oued Fez and Sebou River (Morocco)[END_REF]. The constant use of pesticides and fertilizers by the agricultural activities, plus the connection with untreated sewage from peripheral cities, result in very pollutant loads that contaminate the river to its estuary [START_REF] Perrin | Water quality assessment of highly polluted rivers in a semi-arid Mediterranean zone Oued Fez and Sebou River (Morocco)[END_REF]. This presumable poor health and ecological status of this ecosystem might be inducing a low trematode parasites diversity, opposing to the latitudinal trend. Indeed, trematodes, especially free-living stages, are sensitive to water disturbance, reducing their survival, preventing transmission between hosts [START_REF] Pietrock | Free-living endohelminth stages: at the mercy of environmental conditions[END_REF][START_REF] Koprivnikar | Contaminant effects on host-parasite interactions: atrazine, frogs, and trematodes[END_REF] and can be used as indicators of retrograde condition [START_REF] Mackenzie | Parasites as pollution indicators in marine ecosystems: a proposed early warning system[END_REF]. Therefore, our results showed that such as free-living species, parasitic fauna seems to follow a latitudinal gradient of decreasing species richness from tropical to extra-tropical areas, one of the oldest recognized ecological patterns [START_REF] Wright | Energy supply and patterns of species richness on local and regional scales[END_REF][START_REF] Willig | Latitudinal gradients of biodiversity: Pattern, process, scale, and synthesis[END_REF]. This latitudinal pattern is usually not clear for communities of parasites with complex life cycles [START_REF] Poulin | Latitudinal gradient in the taxonomic composition of parasite communities[END_REF]Studer et al., 2013) due to the complexity of host/ parasite interactions, but also because these cycles (and in particular infection success stage) depend on several abiotic factors, including anthropogenic stressors [START_REF] Rohr | Understanding the net effects of pesticides on amphibian trematode infections[END_REF][START_REF] Altman | Large-scale spatial variation in parasite communities influenced by anthropogenic factors[END_REF].

Among abiotic factors, temperature is one of the strongest drivers of trematode activity (propagule dispersal, survival, infection [START_REF] Thieltges | Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae)[END_REF]) as well as of host infection levels (higher values observed during the warmer seasons [START_REF] Goater | Population biology of Meiogymnophallus minutus (Trematoda: Gymnophallidae) in cockles from the Exe Estuary[END_REF][START_REF] Desclaux | Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis[END_REF])). As an example, in Arcachon bay, a synchrony was observed between parasites emergence from the first intermediate host and the infection in the second intermediate host when water temperature was above 15 °C (de Montaudouin et al., 2016a).

In the case of the present study, the minimum water temperature of the aquatic systems south of 36 °N was around 15°C, 3 °C above north of 36 °N. This temperature difference can explain why Morocco displays higher TTP and TMA than Portugal. In fact, this study showed that abundance and prevalence of trematode communities presented higher values in ecosystems characterized by higher maximum water temperature (affinity group A). In contrast, all the northern sampled areas (Portuguese aquatic systems located north of the strait of Gibraltar) were all gathered in the same affinity group (group B2.2) characterized by the lowest trematode abundance and prevalence. The Portuguese coast proximity to an upwelling front and consequent occurrence of cold vertical currents [START_REF] Queiroz | Spatial dynamics and expanded vertical niche of blue sharks in oceanographic fronts reveal habitat targets for conservation[END_REF] may operate as a shield against trematode infection.

In the present study, the discrimination of the trematode assemblages was also explained by the cockle density, the sediment median grain-size and the type of aquatic system, some of these factors being possible confounding. Cockles density was higher in the studied areas characterized by higher maximum temperature. This can result either from increased recruitment success [START_REF] Gam | Population dynamics and secondary production of the cockle Cerastoderma edule: A comparison between Merja Zerga (Moroccan Atlantic Coast) and Arcachon Bay (French Atlantic Coast)[END_REF][START_REF] Magalhães | Cockle population dynamics: recruitment predicts adult biomass, not the inverse[END_REF] or from better conditions in terms of food quality and quantity. Nevertheless, the system presenting the highest cockle density (Sidi Moussa lagoon) was also the system with one of the lowest trematode abundance suggesting that when a certain density threshold is passed, cercariae are diluted among second intermediate host and consequent lower mean metacercariae infection is observed, as previously highlighted by [START_REF] Magalhães | Cockle population dynamics: recruitment predicts adult biomass, not the inverse[END_REF].

The type of aquatic system (estuaries, lagoons or bays) showed also to be determinant for the trematode community composition. There was a clear separation between three particular areas South of 36 °N, that presented higher trematode biodiversity:

Oualidia and Sidi Moussa lagoon, and Dakhla bay corresponding to group B1 and B2.1, respectively. These areas are classified as coastal lagoons (group B1) or bays (group B2.1)

and therefore characterized by higher oceanic influence and hydrodynamics [START_REF] Kjerfve | Geographic and Hydrodynamic Characteristics of Shallow Coastal Lagoons[END_REF] and lower water temperature variations, especially Dakhla bay which is located in the interaction between the Canary stream and the subtropical ridge currents [START_REF] Orbi | Etude Pluridisciplinaire de la Baie de Dakhla. Note d'information (interne) sur la planification de l'aquaculture dans la baie de Dakhla[END_REF]. [START_REF] Leung | Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: Life cycles, ecological roles and DNA barcodes[END_REF] and Mouritsen and Poulin (2005) referred that these combinations of characteristics are usually related to higher trematode diversity and abundance, which was confirmed by our results (the highest rarefaction indices were found in affinity groups B1 and B2.1). Additionally, coastal lagoons tend to be shallower compared to estuaries [START_REF] Kjerfve | Comparative oceanography of coastal lagoons[END_REF]. This enables light to penetrate up to the bottom, allowing benthic plants to thrive (higher productivity) [START_REF] Kennish | Coastal Lagoons Critical Habitats of Environmental Change[END_REF] which could lead to an increase of benthic communities (first hosts of trematode species) diversity and abundance. As previously discussed, higher hosts diversity and abundance is usually correlated to higher trematode diversity [START_REF] Hechinger | Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts[END_REF].

Cockles from Óbidos lagoon, located 40 °N, displayed extreme values of infection, with the lowest TTP and TMA registered. Most of the hosts of the trematode species found in this study have been previously reported in this lagoon (e.g. [START_REF] Carvalho | Factors structuring temporal and spatial dynamics of macrobenthic communities in a eutrophic coastal lagoon (Óbidos lagoon, Portugal)[END_REF][START_REF] Lourenço | Seasonal abundance of aquatic birds at Óbidos lagoon[END_REF], however this aquatic system presented the lowest values of water temperature, showing once again the great importance that water temperature has on trematode infection. Besides, this system also has the peculiarity that cockles were collected in a subtidal position. Despite this assumption is based on only one sampling point, these results could suggest that cockles tidal position can also be a driver of trematode infection.

In fact, similar results were found by [START_REF] Gam | Metazoan parasites in an intermediate host population near its southern border: The common cockle (Cerastoderma edule) and its trematodes in a Moroccan coastal lagoon (Merja Zerga)[END_REF] in Merja Zerga coastal lagoon (Morocco) where cockles living in subtidal zones presented lower trematode infection that intertidal sympatric specimens. This was interpreted as a differential distance to upstream intertidal first intermediate host.

The temporal gap and the seasonal differences among some of the samples could of course bias our spatial analysis. However, at these scales, we assume that spatial effects (17° in latitude corresponding to approx. 3,000 km) are stronger than temporal effects (8 years), once trematode composition at a given site is often stable at multiannual scale. As an illustration, de [START_REF] De Montaudouin | Assessing parasite community structure in cockles Cerastoderma edule at various spatio-temporal scales[END_REF] showed that trematode communities of Arcachon bay, France, were the same after 8 years, the same temporal gap as in this study, due to environmental stability along time. In the same direction, in the Ria de Aveiro coastal lagoon, one of the sampled systems, diversity of trematode was equivalent after 6 years [START_REF] Freitas | Trematode communities in cockles (Cerastoderma edule) of the Ria de Aveiro (Portugal): Influence of inorganic contamination[END_REF][START_REF] Russell-Pinto | Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro, Portugal[END_REF]. On the other hand, concerning seasonal differences, actually, trematode abundance (infecting cockles as second host) follows a seasonal pattern, increasing their infections during the warmer seasons, contrary to what is observed in the colder seasons [START_REF] Desclaux | Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis[END_REF][START_REF] Goater | Population biology of Meiogymnophallus minutus (Trematoda: Gymnophallidae) in cockles from the Exe Estuary[END_REF]. This could mean a positive influence of the results (in terms of infection intensity) in the Portuguese aquatic systems (systems sampled during summer). However, due to the low trematode abundance on the Portuguese systems, seasonal effects are not so evident [START_REF] Magalhães | Spatio-temporal variation of trematode parasites community in Cerastoderma edule cockles from Ria de Aveiro (Portugal)[END_REF].

Moreover, the present study findings demonstrated a higher trematode abundance on Moroccan aquatic systems (winter samples), which means that seasonal effects were not exacerbated. Finally, we believe that the present findings are of high impact because of the interest in trematode communities knowledge improvement in each sampled area and each country.

CONCLUSION

The present study showed that at the studied scale, trematode abundance and prevalence in cockles seemed to follow a latitudinal pattern. This latitudinal gradient of trematode, however, was more related to temperature than to latitude. In fact, the type of aquatic system, namely coastal lagoons or bays, also demonstrated to have an impact, correlated with the oceanic influence. Nevertheless, the occurrence of trematode species is only possible when all the hosts of that species were present in the ecosystem.

Furthermore, the obtained results highlighted the ubiquity of trematode parasites in the different aquatic systems and alert to a possible change on the trematode fauna composition and abundance in cockle populations driven by thermal modification mediated by oceanographic global circulation. Besides global temperature monitoring, it is then imperative to incorporate trematodes communities assessment in ecological studies, due to their highly integrative significance, to better predict potential negative impact on host populations and communities sustainability. Nonetheless, due to the seasonal and temporal differences between sampling efforts it is important to perform more studies to fully comprehend what drives trematode communities in a latitudinal gradient, along with studies that support temporal consistency in trematode communities.

Fig. 1

 1 Fig. 1 Study area. Geographical location of the 17 aquatic systems distributed along

Fig. 2

 2 Fig. 2 Latitudinal distribution of the 12 trematode species found in Cerastoderma

Fig. 3

 3 Fig.3Trematode mean abundance per aquatic system for the two most

Fig. 4

 4 Fig. 4 Cluster analysis based on trematode parasites communities in seventeen

Fig. 5

 5 Fig. 5 Distance-based redundancy analysis plot and the correlated variables that

  ): group A, subdivided into A1 composed by Tahaddart, Loukkos, Sebou and Souss estuaries and A2 composed by Merja Zerga lagoon, Oum Er Rbia estuary and Khnifiss lagoon; group B, divided in B1 composed by Sidi Moussa and Oualidia lagoons and group B2, splitted into B2.1 composed by Dakhla bay and B2.2composed by all Portuguese systems (Ria de Aveiro lagoon, Óbidos lagoon, Albufeira lagoon, Sado estuary, Mira estuary and Ria Formosa lagoon). Cockle density showed to be significantly higher in group B1 and lower in group B2.1. Sediment median grain-size was significantly higher in group B2.2 and lower in group B2.1 (Table5). Concerning water physico-chemical characterization, all descriptors showed no significant differences among the affinity groups. Nevertheless, group A1 displayed the highest values of maximum and minimum water temperature while, group B2.2 registered the lowest values for the same variables. Maximum and minimum water salinity presented the highest values for group B2.1

  Parvatrema minutum, Curtuteria arguinae and Himasthla interrupta) for which there is no influence of the biogeographical barrier (i.e. Gibraltar) and which occurrence is mediated by the predominant presence of the intermediate hosts in the sampled area (Peringia ulvae,

	Scrobicularia plana, Gobius spp., among others (cf. Table 2)). In this study H. continua was
	only found south of Gibraltar (36 °N), however, its published distribution (de Montaudouin et
	al., 2009) places this species in this ubiquitous group of parasites. The life cycle of C.
	arguinae, is unknown (Desclaux et al., 2006) preventing any hypothesis concerning the link
	with first intermediate and final hosts distribution. M. parvus was only observed at the
	Portuguese coast, still this isolated occurrence is more likely related to the fact that
	trematodes infecting first intermediate host, usually display very low prevalence (Granovitch

The first category gathers seven trematode species (Monorchis parvus, Bucephalus minimus, Psilostomum brevicolle,

Gymnophallus choledochus, and Johannesson, 2000; Islam et al., 2009;[START_REF] Tigga | Prevalence of snail's intermediate host infected with different trematodes cercariae in and around Ranchi[END_REF]

. Indeed, M. parvus has been previously recorded along the whole studied latitudinal gradient

[START_REF] De Montaudouin | Digenean trematode species in the cockle Cerastoderma edule: Identification key and distribution along the North-Eastern Atlantic Shoreline[END_REF]

. The second category, contrastingly, gathers two trematode species with a Southern distribution, Diphterostomum brusinae and H. quissetensis, possibly mediated by the biogeographical barrier and first intermediate host, Tritia reticulata, an abundant gastropod in southern areas, from France to Morocco (but its actual northern latitude corresponds to Baltic Sea

Table 1 .

 1 Characterization of each sampled area in terms of type of aquatic system (1 = lagoon; 2 = estuary; 3 = bay), latitude (LAT), longitude

	(LON), surface area (km 2 ), maximum annual water temperature (M Temp, °C), minimum annual water temperature (m Temp, °C), maximum
	annual water salinity (M Sal), minimum annual water salinity (m Sal) and sediment median grain-size (MGS, mm). ND -no data
	System	Type	LAT (N) LON (W)	Surface Area (km 2 )	M Temp m Temp M Sal m Sal MGS	References
	Ria Aveiro		40°38'	8°44'	83.0	22.0	15.0	28.0	12.0	0.277	Dias et al., 2000 Lillebø et al., 2015
	Óbidos		39°24'	9°12'	7.0	22.0	10.0	37.0	26.0	0.392	Malhadas et al., 2009 Oliveira et al., 2006
	Albufeira		38°30'	9°10'	1.3	22.5	11.0	36.0	31.0	0.404 Fortunato et al., 2014
	Sado		38°28'	8°50'	240.0	21.9	13.8	36.0	10.9	0.304	Bao et al., 1999 Martins et al., 2001
	Mira		37°43'	8°46'	16.0	22.5	12.0	35.0	27.0	0.353 Silva et al., 2006
	Ria Formosa		36°58'	7°52'	170.0	26.0	12.0	36.5	13.0	0.326 Gamito and Erzini, 2005
	Tahaddart		35°46'	5°42'	10.0	26.0	13.0	41.0	21.0	0.194 Achab, 2011
	Loukkos		35°07'	06°00'	72.0	27.0	15.0	34.0	22.0	0.203 Geawhari et al., 2014
	Merja Zerga		34°51'	06°16'	27.0	28.0	11.0	35.0	27.0	0.272 Gam et al., 2010
	Sebou		34°16'	06°39'	17.5	30.0	16.0	35.0	12.0	0.219 Haddout et al., 2015
	Oum Er Rbia		33°28'	08°34'	1.5	25.0	15.0	35.0	30.0	0.146 Khalki and Moncef, 2007
	Sidi Moussa		32°54'	08°49'	4.2	27.0	15.0	33.0	22.0	0.273 Maanan et al., 2004
	Oualidia		32°45'	08°30'	3.0	21.0	16.0	36.0	28.0	0.181 Hilmi et al., 2005
	Souss		30°21'	09°35'	16.0	25.0	19.0	39.0	35.0	0.202 Anaijar et al., 2008

Table 4 .

 4 Prevalence of trematode parasites infecting cockle populations in the aquatic systems of Portugal and Morocco. Sampling sites: RA -Ria de Aveiro; OB -Óbidos lagoon; AL -Albufeira lagoon; SA -Sado estuary; MI -Mira estuary; RF -Ria Formosa; TA -Tahaddart estuary; LO -Loukkos estuary; MZ -Merja Zerga lagoon; SE -Sebou estuary; OR -Oum Er Rbia estuary; SM -Sidi Moussa lagoon; OA -Oualidia lagoon; SO -Souss estuary; CH -Chbika estuary; KH -Khnifiss lagoon and DA -Dakhla bay. N: number of dissected cockles.

			B. minimus	M. parvus	G. choledochus	D. brusinae	H. continua	H. elongata	H. interrupta	H. quissetensis	C. arguinae	P. brevicolle	P. minutum	R. roscovitus	Total parasite	Prevalence
		RA (n=65)	_	_	_	_	_	11	_	_	_	_	26	_	35
		OB (n=35)	3	_	_	_	_	_	_	_	_	_	_	3	6
	Portugal	AL (n=20) SA (n=21)	_ _	40 _	_ _	20 _	_ _	10 48	_ 5	_ _	_ _	_ _	_ _	_ _	55 52
		MI (n=20)	_	_	50	_	_	_	_	_	_	5	_	_	55
		RF (n=25)	_	_	_	4	_	_	_	36	20	4	8	_	48
		TA (n=13)	8	_	_	15	54	_	_	_	_	_	100	_	100
	Morocco	LO (n=20)	10	_	_	10	_	_	_	_	_	_	90	_	90
		MZ (n=20)	_	_	_	30	_	_	_	70 100	_	100	_	100

Table 5 .

 5 Characterization of each affinity group in terms of maximum annual water temperature (M Temp, °C), minimum annual water temperature (m Temp, °C), maximum annual water salinity (M Sal), minimum annual water salinity (m Sal), sediment median grain size (MGS, mm), cockles density (ind.m -2 ) and Rarefaction index for a standardized number of 10 individuals (ES(10)). Significant differences among affinity groups are represented with different letters (p < 0.05). Sampling sites: RA -Ria de Aveiro; OB -Óbidos lagoon; AL -Albufeira lagoon; SA -Sado estuary; MI -Mira estuary; RF -Ria Formosa; TA -Tahaddart estuary; LO -Loukkos estuary; MZ -Merja Zerga lagoon; SE -Sebou estuary; OR -Oum Er Rbia estuary; SM -Sidi Moussa lagoon; OA -Oualidia lagoon; SO -Souss estuary; CH -Chbika estuary; KH -Khnifiss lagoon and DA -Dakhla bay.

	Affinity groups	Sampling areas	M Temp	m Temp	M Sal	m Sal	MGS	Cockle density	ES (10)
	A1	TA, LO, SE, SO	27.0 ± 2.2	15.8 ± 2.5	37.3 ± 3.3	22.5 ± 9.5	0.2 ± 0.0 a	404 ± 457 a	1.0
	A2	MZ, OR, KH	25.0 ± 3.0	14.0 ± 2.6	36.0 ± 1.7	30.3 ± 3.5	0.2 ± 0.1 a,b	1643 ± 2267 a,b	1.3
	B1	SM, OA	24.0 ± 4.2	15.5 ± 0.7	34.5 ± 2.1	25.0 ± 4.2	0.2 ± 0.1 a,b	6092 ± 1114 b	2.4
	B2.1	DA	26.0	14.0	39.5	37.0	0.1 b	15 c	2.4
	B2.2	RA, OB, AL, SA, MI, RF	22.8 ± 1.6	12.3 ± 1.8	34.8 ± 3.4	20.0 ± 9.0	0.3 ± 0.0 c	135 ± 304 a	1.0

Table 6 .

 6 Results of the Similarity Percentages (SIMPER) used to characterize the type of aquatic systems (coastal lagoons vs. estuaries) and the geographical position (northern systems vs. southern systems) by the trematode species (of Cerastoderma edule) that most contributed to dissimilarity between groups.

	Species	Average abundance group 1 Average abundance group 2 Dissimilarity Contribution (%)
	Parvatrema minutum	5.42	12.22	69.28
	Himasthla quissetensis	1.70	0.00	8.76
	Coastal lagoons (1) vs
	Himasthla interrupta	0.66	0.29	4.64
	Estuaries (2)
	Curtuteria arguinae	0.91	0.00	3.83
	Himathla elongata	0.05	0.13	3.74
	Species	Average

abundance group 1 Average abundance group 2 Dissimilarity Contribution (%) Northern systems (1) vs Southern systems (2)

	Parvatrema minutum	0.84	13.15	58.62
	Himasthla quissetensis	0.06	1.81	10.26
	Dipheterostomum brusinae	0.04	1.04	9.12
	Curtuteria arguinae	0.00	1.30	8.48
	Himasthla interrupta	0.01	0.99	6.02

Acknowledgments

This work was supported by the research project COCKLES (EAPA_458/2016 COCKLES Co-Operation for Restoring CocKle SheLlfisheries & its Ecosystem-Services in the Atlantic Area) and by the financial support from the project 18571 CNRST (Morocco) -CNRS (France). Simão Correia and Luísa Magalhães benefited from research fellowships funded by 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). Rosa Freitas was funded by national funds (OE), through FCT -Fundação para a Ciência e a Tecnologia, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. Thanks are also due to FCT/MCTES for the financial support to CESAM (UID/AMB/50017/2019), through national funds.

Authors are thankful to all the institutions and fishermen that contributed for the accomplishment of this study.

Highlights

Trematode diversity in the southern distribution area of Cerastoderma edule.

Trematode species occurrence driven by the presence of the first intermediate host.

Trematode prevalence and abundance was positively correlated to temperature.

At large scale, cockle density positively influences trematode abundance.

Systems under buffered environmental variations presented higher trematode abundance.

Cockle density influences positively trematode abundance within certain values

Declaration of interests

☒ 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.

☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:


Ana O Paixao

Fabricar

Armando Silva Carvalho

Ana Paixão

Keywords: composition au féminin, compositrices, musique portugaise contemporaine

come

O fabricar da música e do silêncio [La fabrication de la musique et du silence] : Clotilde Rosa et la composition au féminin au Portugal

Vermeer se trouvait chez elle dans le 'foyer musical' des Duarte» 2 . Au-delà du père Gaspar, la soeur de Diego, Leonora Duarte, est aussi devenue compositrice de renommée et la partition de sept de ses symphonies est arrivée jusqu'à nos jours [START_REF]l'âge de 44 ans va écrire sa première oeuvre s'émancipant de ses activités d'interprète et d'enseignante, composant plus de 70 oeuvres, certaines d'entre elles enregistrées, comme nous pouvons le voir. Même si les performers et les professeurs au féminin continuent d'exceller, il y a un changement de paradigme, symbolisé par Clotilde Rosa, faisant sortir les femmes de leurs rôles traditionnels d'enseignement et d'interprétation. Et la nouvelle génération de compositrices n'est que le début d'une vague féminine qui progressivement s'installe dans la musique portugaise[END_REF] . Celui-ci n'est que l'un des noms de compositrices qui a été effacé par le temps et par les recherches musicologiques.

Tacet 4

Faisant la déconstruction d'un titre de Derrida 5 , où la voix garde le silence, nous pourrons dire l'inverse à propos de la présence féminine dans la musique, portugaise ou autre: à quel point la construction historique a caché, oublié, la voix, la présence de femmes artistes de relief, telles que Leonora Duarte ?

Comme le souligne Heidegger : 1 Cf. Rudolf Rasch, The Antwerp Duarte Family as Musical Patrons" in Orlandus Lassus and his Time, Colloquium Proceedings Antwerpen 24.-26.08.1994. Alamire Foundation 1995, pp. 424-425. 2 Edwin Buijsen, "Music in the Age of Vermeer," in M. C. van der Sman (ed.), Dutch Society in the Age of Vermeer, Zwolle 1996, p. 118. Notre traduction. [START_REF]l'âge de 44 ans va écrire sa première oeuvre s'émancipant de ses activités d'interprète et d'enseignante, composant plus de 70 oeuvres, certaines d'entre elles enregistrées, comme nous pouvons le voir. Même si les performers et les professeurs au féminin continuent d'exceller, il y a un changement de paradigme, symbolisé par Clotilde Rosa, faisant sortir les femmes de leurs rôles traditionnels d'enseignement et d'interprétation. Et la nouvelle génération de compositrices n'est que le début d'une vague féminine qui progressivement s'installe dans la musique portugaise[END_REF] Cf. Manuscrit 429, au Christ Church College à Oxford, contient sept Sinfonias de Leonora Duarte. Les en-têtes sont de la main de Gaspar Duarte, père. 4 Tacet -terme musical pour indiquer à un instrumentiste qu'il doit rester silencieux pendant toute la durée du mouvement ou pendant un fragment assez long. Tacet, en latin, signifie «il se tait», «on se tait». 5 Déconstruction du titre d'un des chapitres de Jacques Derrida en La voix et le phénomène. Paris : PUF, 2012, p. 83.

Entendre ce qui est sans voix demande une ouïe <qui> ne dépend pas seulement de l'oreille, mais aussi de l'appartenance de l'homme à Ce à quoi son être est accordé6 .

Ecouter la voix des femmes artistes, vouée au silence par la construction historique va exiger une oreille qui souhaite s'accorder, être en consonance, chercher ces voix féminines. Tendre une «troisième oreille»7 nietzschéenne, pour écouter, pour savoir écouter et donner à entendre les musiciennes, compositrices, performers du passé. Faire émerger la voix féminine du silence est justement l'un des objectifs de la recherche musicologique actuelle.

Les femmes artistes inconnues du passé n'existent pas

Des projets de recherche révèlent de plus en plus l'existence d'un passé musical au Portugal avec des exemples féminins. Il suffit de penser au travail de la musicologue Manuela Paraíso sur la présence de femmes dans la musique portugaise ou de la recherche de Helena Lopes Braga sur le Au-delà de son travail de fabrication musicale, Clotilde Rosa est, avec son mari Carlos Franco, personnalité de référence dans le domaine de la diffusion de la musique contemporaine au Portugal.

Clotilde inverse ainsi le paradigme de la femme-performer, de la femme-pédagogue, devenant femme-divulgateur, femme-compositeur. Et c'est précisément l'une de ses compositions que nous analyserons.

O fabricar da música e do silêncio

En 1977, Armando Silva Carvalho publie Armas brancas: poema quase dramático 13 Tropeço: acaso um homem voa? Pergunto: mas que auto nos move a nós, artistas musicais.

As almas

Diz-se que as almas não suportam uma música espessa Que se afastam entre as cordas de pianos fúteis Que deslizam como peixes ofendidos pelas malhas intrincadas de certas partituras.

As almas sentaram-se no chão. Lembro-me que falavam baixo entre a folhagem e apenas pretendiam descansar. E os homens escondiam das visitas essas fúteis fabricantes do silêncio.

Entre dentes

  silence qui garde la voix» Du catalogue du collectionneur et marchant d'art Diego Duarte établi en 1682 faisait partie le tableau de Vermeer, Dame assise au virginal 1 . Diego Duarte était l'un des 8 enfants du couple juif portugais refugié à Anvers -Gaspar et Catarina Duarte -, et d'au-delà d'un intérêt par les beaux-arts, quelques éléments de la famille jouaient des instruments ou étaient compositeurs, comme c'est le cas de Gaspar Duarte. La collection de son fils Diego présente quelques tableaux à thématique bien précise qui «[…] ont été appellatifs pour Diego Duarte du point de vue de leur nature musicale… Et c'est le cas du nombre 182 de la liste, Dame assise au Clavesingel [virginal] par Vermeer, sa nature musicale a certainement joué un rôle pour son achat. Certainement que la 'pièce musicale' de

  même sujet pendant le XX e siècle. Mais aussi, concernant la musique féminine du XX e siècle, le rôle fondamental du Groupe de Musique Contemporaine de Lisbonne, qui a eu des femmes comme Constança Capdeville ou Clotilde Rosa à son origine, un groupe qui a fait connaître les oeuvres de beaucoup de compositrices et intégré beaucoup de femmes interprètes. Les recherches et les performances de musique contemporaine ont permis, par exemple, de souligner les rôles des compositrices Berta Alves de Sousa (1906-1997) (et ses expériences dans le champ de la composition en symétrie sonore) et Francine Benoît (1894-1990) (née en France, mais arrive au Portugal en 1906) qui côtoient une génération de jeunes compositrices comme Elvira de Freitas (1928-), Maria Teresa Macedo (1917-), Isabel Lupi e Natércia Couto (1924-1999). Sans oublier, bien sûr, les «révolutions silencieuses» de Constança Capdeville (1937-1992) (nom majeur de la composition portugaise avec plusieurs prix de composition notamment pour son oeuvre Variations sur le nom de Stravinsky), Maria de Lourdes Martins (1926-1999) (prix de composition de la FCG pour O Encoberto (1965) et O Litoral (1971)) et Clotilde Rosa (1930-). Toutes ces compositrices du XX e siècle mentionnées seront simultanément grandes professeures, divulgatrices, performers, continuant à jouer le rôle plus représenté par les femmes dans la musique portugaise -celui de grandes pédagogues ou interprètes. sociales à la professionnalisation féminine, le poids des responsabilités familiales et domestiques ont été des facteurs d'entrave à la parution de femmes artistes. A part les exemples parsemés que nous venons de voir et ceux que la recherche musicologique est en train de révéler, la fabrique et la pratique de la musique au féminin sont dominées par un silence que les XXe et XXIe siècles combleront, comme le parcours de Clotilde Rosa le montre. Après avoir fréquenté les Cursus de Darmstadt et d'une carrière d'harpiste, de performer et de pédagogue de plus de 20 ans, Clotilde Rosa écrira tardivement sa première oeuvre en 1974, Incon-sub-sequência, ce qui ne l'empêchera pourtant pas de créer plus de 70 oeuvres jusqu'à présent.

  , reccueil qui inclut les poèmes «O fabricar da música», «As almas» et «Entre dentes». Trois textes qui auront une traduction intersémiotique de Clotilde Rosa en 1987. La compositrice s'intéresse aux rapports entre la musique et la poésie : Tout au long de mon oeuvre la poésie a toujours été présente, puisque la Poésie pour mon esprit est de la Musique aussi. Notre culture portugaise est pleinement peuplée de poètes; comment pourrais-je en tant que compositrice, m'aliéner d'une telle richesse? 14 Et c'est justement en quête de cette richesse, et insistant sur les caractéristiques musicales du mot poétique, que Clotilde Rosa utilise les textes suivants d'Armando Silva Carvalho comme point de départ de sa traduction intersémiotique: O fabricar da música Aonde ponho as mãos há um sinal usado e poucos são nas salas os metais. Deslizo com a dor pelo corredor com teclas ancestrais.

Martin Heidegger, Le principe de raison, préface de Jean Beaufret et traduction d'André Préau. Paris, Gallimard : 1983, p. 129.

Friedrich Nietzsche, Par-delà le Bien et le Mal. Traduction d'Angèle Marietti. Paris: Poche, 2000, §246.

Armando Silva Carvalho, Armas Brancas: poema quase dramático. Porto: Limiar Editora, 1977.

Clotilde Rosa, Musica para poesia portuguesa, Booklet CD. Grupo de Música Contemporânea de Lisboa. Lisboa: La ma de Guido, 2010, p. 3. Notre traduction.

Clotilde Rosa, Musica para poesia portuguesa, Booklet CD. Grupo de Música Contemporânea de Lisboa. Lisboa: La ma deGuido, 2010, p. 14.