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Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline

Published online by Cambridge University Press:  26 March 2009

Xavier de Montaudouin ,
David W. Thieltges ,
Mériame Gam ,
Manuela Krakau ,
Suzana Pina ,
Hocein Bazairi ,
Laurent Dabouineau ,
Fernanda Russell-Pinto  and
K. Thomas Jensen
Xavier de Montaudouin*
Affiliation:
Université de Bordeaux, UMR EPOC 5805, Station Marine d'Arcachon, 2 rue du Pr Jolyet, F-33120 Arcachon, France
David W. Thieltges
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
Mériame Gam
Affiliation:
Université Hassan II Aïn Chock, Faculté des Sciences Aïn Chock, Départment de Biologie, Km 8 Route El Jadida, BP 5366 Maârif, 20100 CasablancaMorocco
Manuela Krakau
Affiliation:
Foundation Alfred Wegener Institute for Polar and Marine Research, Wadden Sea Station Sylt, Hafenstraße 43, 25992 List/Sylt, Germany
Suzana Pina
Affiliation:
Laboratory of Aquatic Zoology, Department of Aquatic Production, ICBAS, Abel Salazar Institute for Biomedical SciencesLg. Prof. Abel Salazar 2, 4009-003 Porto, Portugal
Hocein Bazairi
Affiliation:
Université Hassan II Aïn Chock, Faculté des Sciences Aïn Chock, Départment de Biologie, Km 8 Route El Jadida, BP 5366 Maârif, 20100 CasablancaMorocco
Laurent Dabouineau
Affiliation:
Campus de la Tour d'Auvergne BP 90431, Université UCO Bretagne Nord, 22 204 Guingamp, France
Fernanda Russell-Pinto
Affiliation:
Laboratory of Aquatic Zoology, Department of Aquatic Production, ICBAS, Abel Salazar Institute for Biomedical SciencesLg. Prof. Abel Salazar 2, 4009-003 Porto, Portugal
K. Thomas Jensen
Affiliation:
Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Finlandsgade 14, DK-8200 Aarhus, Denmark
*
Correspondence should be addressed to: X. de Montaudouin, Université de Bordeaux, UMR EPOC 5805, Station Marine d'Arcachon 2 rue du Pr Jolyet, F-33120 Arcachon, France email: x.de-montaudouin@epoc.u-bordeaux1.fr
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Abstract

We describe the digenean fauna of one of the dominant intertidal hosts, the common cockle Cerastoderma edule, in terms of biomass, off north-eastern Atlantic shores. Using published and unpublished literature we have prepared an identification key and provide an up-date of the large-scale distributional patterns of digenean species of the common cockle. At least sixteen digenean species, belonging to seven families, use cockles as intermediate host. Among these species two utilize cockles as first intermediate host only, whereas two species utilize cockles as both first and second intermediate host. The remaining eleven species have cockles as their second intermediate host. Water birds and fish are the definitive hosts to twelve and four species, respectively.

Cockles are infected with digeneans along the latitudinal gradient from southern Morocco to the western region of the Barents Sea often with high infection levels. Whereas some of these digenean species occur along most of the latitudinal gradient others show a more restricted northern or southern distribution mostly caused by an underlying latitudinal gradient of host species.

Knowledge of digenean species and their large-scale distribution pattern may serve as a baseline for future studies dealing with the effects of climate change on parasite–host systems. For such studies the cockle and its digenean community could be an ideal model system.

Keywords

parasitismlatitudinal patternsCerastoderma eduleidentification key
Type
Review
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 3 , May 2009 , pp. 543 - 556
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

INTRODUCTION

Although parasite diversity is supposed to be high (Windsor, Reference Windsor1998; Poulin & Morand, Reference Poulin and Morand2000), our knowledge of parasite diversity and latitudinal patterns is limited (Littlewood, Reference Littlewood and Rohde2005). In intertidal ecosystems, digeneans are the dominant parasite group (Mouritsen & Poulin, Reference Mouritsen and Poulin2002). They play a double function being part of the living diversity, but at the same time they can also play the role as diversity indicators because their presence is linked to the occurrence of free-living fauna (their hosts) (Mouritsen & Poulin, Reference Mouritsen and Poulin2002; Hechinger & Lafferty, Reference Hechinger and Lafferty2005; Hudson et al., Reference Hudson, Dobson and Lafferty2006; Hechinger et al., Reference Hechinger, Lafferty, Huspeni, Brooks and Kuris2007). Knowledge of parasite diversity is thus not only valuable in itself in assessing a neglected part of biodiversity but it might also serve as a valuable and convenient proxy for ecosystem health (Hudson et al., Reference Hudson, Dobson and Lafferty2006). As many digeneans have been shown to affect host individuals, populations and communities (Mouritsen & Poulin, Reference Mouritsen and Poulin2002) knowledge of parasite distributional patterns in host populations can contribute to an understanding of their role in shaping population dynamics in their free-living hosts. Parasite–host interactions may be influenced by climate change because parasite transmission and parasite effects on their host closely depend on temperature (Evans, Reference Evans1985; Sousa & Gleason, Reference Sousa and Gleason1989; Jensen et al., Reference Jensen, Latama and Mouritsen1996; Lo & Lee, Reference Lo and Lee1996; Mouritsen & Jensen, Reference Mouritsen and Jensen1997; Ferrell et al., Reference Ferrell, Negovetich and Wetzel2001; Mouritsen, Reference Mouritsen2002; Thieltges & Rick, Reference Thieltges and Rick2006). Hence, climate change could disrupt equilibrium in parasite–host relationships and beget serious mortalities (Hayes et al., Reference Hayes, Bonaventura, Mitchell, Prospero, Shinn, Van Dolah and Barber2001; Kutz et al., Reference Kutz, Hoberg, Polley and Jenkins2005; Mouritsen et al., Reference Mouritsen, Tompkins and Poulin2005; Hakalahti et al., Reference Hakalahti, Karvonen and Valtonen2006; Poulin, Reference Poulin2006; Poulin & Mouritsen, Reference Poulin and Mouritsen2006). In addition, the introduction or range expansion of parasite species in the course of warming seas might increase the parasite burden for intertidal hosts. To evaluate future changes, inventories of parasite diversity over the distributional range of a particular host (parasite fauna) will be necessary to serve as a baseline. Today, no such inventories exist for hosts from intertidal systems.

The edible cockle Cerastoderma edule from the north-eastern Atlantic shoreline, probably harbours one of the most diverse digenean faunas of bivalve hosts in intertidal systems (Lauckner, Reference Lauckner and Kinne1983; de Montaudouin et al., Reference de Montaudouin, Kisielewski, Bachelet and Desclaux2000; Thieltges et al., Reference Thieltges, Krakau, Andresen, Fottner and Reise2006). Cockles are first or second intermediate hosts to at least 16 parasite species. These digeneans display complex life cycles involving 2–3 host species. The cockle parasites are using either water birds or fish as definitive hosts (for a general description of life cycles of digeneans see Smyth, Reference Smyth1994). By using reported characteristics and morphometric recordings we present an identification key to the digeneans found in cockles along its latitudinal distributional area. Their overall biogeographical distribution is described and we discuss possible causative factors for the observed patterns.

MATERIALS AND METHODS

We searched the literature for information on digeneans using the common cockle Cerastoderma edule as host (Table 1). From the papers on species descriptions we prepared a simple identification key. In addition, photographs of each parasite species as seen through a dissection microscope are provided as a tool for species identification. Approximately fifty publications provided data about the presence of parasite species in cockles and most of them did also report prevalence and/or abundance data for the parasites. Prevalence is the percentage of parasitized cockles and abundance is the number of parasites per cockle (Bush et al., Reference Bush, Lafferty, Lotz and Shostak1997). For each paper, we selected the maximum mean prevalence for species using the cockle as first intermediate host and the maximum mean abundance for species using the cockle as second intermediate host. Comparison between sites must take into account that data were obtained in many different sampling strategies (sample surface, number of replicates and sieve mesh size) and at different times of the year that were not always mentioned. The resulting database includes 45 sites ranging from Dakhla (Morocco, 23°N) to Bodø (Norway, 67°N) (Figure 1).

Fig. 1. Locations from where we found data on parasites in cockles Cerastoderma edule.

Table 1. List of digenean species utilizing the cockle Cerastoderma edule as their first and/or second intermediate host, other hosts of the life cycle, and references to papers describing their anatomy.

(F), fish host; (B), waterbird host.

1: Maillard, Reference Maillard1976; 2: Pina et al., in press; 3: Russell-Pinto et al., Reference Russell-Pinto, Gonçalves and Bowers2006; 4: Bartoli et al., Reference Bartoli, Jousson and Russell-Pinto2000; 5: Jonsson & André, Reference Jonsson and André1992; 6: Lauckner, Reference Lauckner and Kinne1983; 7: Russell-Pinto, Reference Russell-Pinto1993; 8: Sannia et al., Reference Sannia, James and Bowers1978; 9: Lauckner, Reference Lauckner1971; 10: Loos-Frank, Reference Loos-Frank1969; 11: Markowski, Reference Markowski1936; 12: Reimer, Reference Reimer1970; 13: Reimer, Reference Reimer1973; 14: Desclaux, Reference Desclaux2003; 15: Desclaux et al., Reference Desclaux, Russell-Pinto, de Montaudouin and Bachelet2006; 16: Pina, unpublished; 17: Prévot, Reference Prévot1966; 18: Werding, Reference Werding1969; 19: Stunkard, Reference Stunkard1938; 20: Bowers et al., Reference Bowers, Bartoli and James1990; 21: Bowers et al., Reference Bowers, Bartoli, Russell-Pinto and James1996; 22: Russell-Pinto & Bartoli, Reference Russell-Pinto and Bartoli1992; 23: Russell-Pinto & Bowers, Reference Russell-Pinto and Bowers1998; 24: Russell-Pinto, Reference Russell-Pinto1993; 25: Bowers & James, Reference Bowers and James1967; 26: Loos-Frank, Reference Loos-Frank1971; 27: Loos-Frank, Reference Loos-Frank1968.

RESULTS

Identification key

In total, sixteen digenean species have been described from cockles along its north-eastern Atlantic distributional range and one new hitherto undescribed species has been observed in Dahkla (Morocco). The identification key below is based on the appearance of larval digeneans in cockles as seen through a dissection microscope. To facilitate identification of the digeneans, photographs of the individual species are presented (Figure 2). Most of the digeneans in cockles have tissue-specific (=microhabitat) infection sites (Figure 3) and hence location in situ can be of additional help in identification. For each species there is a reference to its distributional area.

Fig. 2. Photographs of digenean larvae as they can be observed through a dissection microscope with transmitted light, within cockle tissues squeezed between two glass slides.

Fig. 3. In situ location of the parasites infecting Cerastoderma edule. When mature, Gymnophallus choledochus, Bucephalus minimus and Monorchis parvus can invade most tissues.

Distributional maps of the individual digenean species are presented in Figure 4.

Fig. 4. [See next page for Figure 4] Distribution of digenean species along the distribution of their cockle Cerastoderma edule host, in the north-eastern Atlantic. P, maximum mean parasite prevalence observed; A, maximum mean parasite abundance observed. Numbers correspond to the following references: 1. Pelseneer, Reference Pelseneer1906; 2. Vaullegard, Reference Vaullegeard1894; 3. Lebour, Reference Lebour1911; 4. James & Bowers, Reference James and Bowers1967; 5. James et al., Reference James, Sannia, Bowers, Nelson-Smith and Bridges1977; 6. Bowers, Reference Bowers1969; 7. Deltreil & His, Reference Deltreil and His1972; 8. Desclaux et al., Reference Desclaux, de Montaudouin and Bachelet2002; 9. Baudrimont et al., Reference Baudrimont, de Montaudouin and Palvadeau2006; 10. Sauriau, Reference Sauriau1992; 11. de Montaudouin et al., Reference de Montaudouin, Kisielewski, Bachelet and Desclaux2000; 12. Russell-Pinto et al., Reference Russell-Pinto, Gonçalves and Bowers2006; 13. Thieltges & Reise, Reference Thieltges and Reise2006; 14. Gam et al., Reference Gam, Bazaïri, Jensen and de Montaudouin2008; 15. de Montaudouin, unpublished; 16. Hancock & Urquart, Reference Hancock and Urquhart1965; 17. Boyden, Reference Boyden1971; 18. Malek, Reference Malek2001; 19. Sannia & James, Reference Sannia and James1978; 20. Sannia et al., Reference Sannia, James and Bowers1978; 21. Jonsson & André, 1992; 22. Thieltges et al., Reference Thieltges, Krakau, Andresen, Fottner and Reise2006; 23. Thieltges, Reference Thieltges2006; 24. Lauckner, Reference Lauckner1971; 25. Jonstone, 1904 (in Lebour, Reference Lebour1911); 26. Bowers & James, Reference Bowers and James1967; 27. Bowers et al., 1990; 28. Goater, Reference Goater1993; 29. Krakau et al., Reference Krakau, Thieltges and Reise2006; 30. Lauckner, Reference Lauckner1984; 31. Russell-Pinto, Reference Russell-Pinto1990; 32. Russell-Pinto & Bartoli, Reference Russell-Pinto and Bartoli1992; 33. Desclaux et al., Reference Desclaux, de Montaudouin and Bachelet2004; 34. Wegeberg & Jensen, Reference Wegeberg and Jensen1999; 35. Wegeberg & Jensen, Reference Wegeberg and Jensen2003; 36. de Montaudouin et al., Reference de Montaudouin, Jensen, Desclaux, Wegeberg and Sajus2005; 37. Desclaux et al., Reference Desclaux, Russell-Pinto, de Montaudouin and Bachelet2006; 38. Kesting et al., Reference Kesting, Gollasch and Zander1996; 39. Loos-Frank, Reference Loos-Frank1971; 40. Loos-Frank, Reference Loos-Frank1969; 41. Thieltges & Reise, Reference Thieltges and Reise2007; 42. Lassalle et al., Reference Lassalle, de Montaudouin, Soudant and Paillard2007; 43. Goater, Reference Goater1995; 44. Reimer, Reference Reimer1970; 45. Bazairi, unpublished; 46. Dang, unpublished 47. Bartoli et al., Reference Bartoli, Jousson and Russell-Pinto2000; 48. Krakau, unpublished; 49. Jensen, unpublished.

KEY TO LARVAL DIGENEANS IN CERASTODERMA EDULE

  1.  –  Isolated, spherical or oval-shaped individuals (= metacercariae), sometimes included in a cyst. Usually gathered in one or two specific tissue(s) 1

  2.  –  Proliferating individuals (×1000), entangled in most tissues when mature. Different forms can be present: small bags (sporocysts or rediae), more or less motile individuals (cercariae) and metacercariae 10

  3. 1 – No cyst, oval shaped 2

  4.  –  Cyst, rather spherical 4

  5. 2 –  Occurring along the margin of the mantle or below the hinge, rather dark through transmitted light (well developed system). Body length 120–300 µm 3

  6.  –  Between adductor muscle and shell, whitish through transmitted light (small excretory system). Body length: 208–482 µm.   Gymnophallus gibberosus (Figure 2A)

  7. 3 –  Enclosed in the mantle epithelium below the shell umbo, between the shell and the flesh, body length 240–350 µm   Meiogymnophallus minutus (Figure 2B)

  8.  –  Free in the extra-pallial space, or under the hinge ligament, but also in the tissues of the mantle margins. Body length: 250–330 µm   Meiogymnophallus fossarum (Figure 2C)

  9. 4 –  Diameter < 160 µm 5

  10.  –  Diameter >160 µm 6

  11. 5 –  Dark excretory vesicles across the whole cyst. Sometimes in the foot (proximal part) but more typically in the thin grey part of the mantle (in compound microscope: with 33 oral spines). Diameter 140–160 µm   Curtuteria arguinae (Figure 2D)

  12.  –  Dark excretory vesicle concentrated and looking as dark spot in a light cyst. Diameter: 140 µm   Diphterostomum brusinae (Figure 2E)

  13.  –  Light excretory vesicles across the whole cyst. Cysts often in the mantle margin opposite of the siphons (anterior end) (microscope: 29 oral spines). Diameter: 80–140 µm Himasthla interrupta (Figure 2F)

  14. 6 –  Thick cyst wall (6–8 µm). Mostly in the palps. Diameter = 160–180 µm   Renicola roscovita (Figure 2G)

  15.  –  No thick cyst wall 7

  16. 7 –  The whole surface of the cyst is blackish-greyish with a net-like structure of the excretory system. Often associated with the digestive gland. Diameter 200–250 µm Psilostomum brevicolle (Figure 2H)

  17.  –  Not these characters 8

  18. 8 –  Diameter > 210 µm. Mainly located in the foot, but sometimes a few in the mantle (microscope: 29 oral spines). Diameter: 210–270 µm   Himasthla elongata (Figure 2I)

  19.  –  Diameter > 290 µm. Located in digestive gland, gills, mantle. Diameter: 300–330 µm   Asymphylodora demeli (Lauckner, Reference Lauckner and Kinne1983, p. 692)

  20.  –  Diameter < 210 µm. Usually located in the foot but sometimes in the mantle. Two species that are impossible to distinguish from each other with a binocular microscope 9

  21. 9 –  Diameter: 150–210 µm (microscope: 29 oral spines)   Himasthla continua (Figure 2J)

  22.    –  Diameter: 150–210 µm (microscope: 31 oral spines) Himasthla quissetensis (Figure 2K)

  23. 10 – Metacercariae within or near sporocysts and cercariae  11

  24. –  Cercariae within or near sporocysts 12

  25. 11 –  Conspicuous excretory vesicle. No cyst. Ovoid (350 x 850 µm) Gymnophallus choledochus (Figure 2L)

  26.  –  No conspicuous excretory vesicle. Cyst. Ovoid (183 x 298 µm) Monorchis parvus (Figure 2M)

  27. 12 –  Cercariae are ovoid with a little tail (66–81 µm). Body length: 91–120 µm Monorchis parvus (Figure 2 N)

  28.  –  Cercariae with a conspicuous tail 13

  29. 13 –  Bifurcate tail 14

  30.  –  Tail not bifurcate. Body length: 300–350 µm   Unknown cercariae (Figure 2P)

  31. 14 –  Tail with a muscular and glandular central stem ended by two long and thin arms. Body length: 300–350 µm   Bucephalus minimus (Figure 2Q)

  32.  –  Rather thick tail, bifurcate from the second half of the tail. Body length: 208–282 µm   Gymnophallus choledochus (Figure 2O)

Host and microhabitat use

Sixteen digeneans, belonging to seven families, have been registered in the edible cockle Cerastoderma edule from the area spanning from southern Morocco to Norway (Table 1). The Echinostomatidae is represented by most species (5). Two of the parasite species utilize the cockle as first intermediate host only (including an undescribed species found in Dakhla 2007, Morocco), eleven as second intermediate host only, and two species as first and second intermediate host (Table 1). The parasites exhibit an aggregated distribution inside the cockle by showing microhabitat specific occurrences (Figure 3). Parasite species utilizing the cockle as first intermediate host usually infect the gonads but as they multiply they proliferate to other microhabitats, especially gills, digestive gland and foot. For parasite species utilizing the cockle as second intermediate hosts, most of them are tissue-specific, but some of the Echinostomatid species may infect both the mantle and the foot. As indicated in Figure 3 the different types of microhabitats are targeted by a varying number of species, the connective tissue in the foot being attractive to 5 species.

Prevalence and abundance

Cockles were infected with parasites at all sites from where data were available (Figure 1). In addition, infection levels observed at the different sites were often high, reaching more than 15% in parasites utilizing cockles as first intermediate hosts (Figure 4A–D). All parasite species using cockles as second intermediate host often have prevalence close to 100% and differ by their metacercariae abundance per host individual (Figure 4E–O). Some parasite species have generally low abundance, i.e. less than 100 metacercariae per cockle, such as Diphterostomum brusinae, Himasthla continua, Gymnophallus gibberosus and Psilostomum brevicolle (Figure 4E, 4H, 4M, 4O). Others may have, in some locations, very high abundance (>100 or 1000) such as Himasthla elongata, H. quissetensis, H. interrupta, Curtuteria arguinae and Renicola roscovita (Figure 4F, 4G, 4I, 4J, 4N). Finally, Meiogymnophallus minutus appears as the most abundant and widespread parasite (Figure 4K).

Latitudinal distribution patterns

Although cockles are infected with digeneans along their entire distributional range, the parasite communities within cockle populations are not the same everywhere. Some parasite species show restricted latitudinal distribution (Figure 4). The unknown cercariae, Diphterostomum brusinae and Curtuteria arguinae display a rather southern distribution (<50°N) while Renicola roscovita, Gymnophallus gibberosus and Asymphylodora demeli display a rather northern distribution (>40°N). Meiogymnophallus minutus and Psilostomum brevicolle occupy the largest latitudinal distribution (40°).

DISCUSSION

Although cockles are infected with digeneans along their entire distributional range, the parasite communities within cockle populations are not the same everywhere. Some parasite species show restricted latitudinal distribution. The latitudinal distributions of first intermediate hosts are important for understanding the patterns of digenean species in cockles. For example metacercariae of Gymnophallus gibberosus, Himasthla elongata and Renicola roscovita occur primarily in the northern part of the cockles' range while metacercariae of Diphterostomum brusinae and Curtuteria arguinae occur exclusively in the south (Figure 4). The northern distribution of G. gibberosus is correlated with the general distribution of the first intermediate host Macoma balthica (north of the Gironde estuary, exceptionally Arcachon Bay, France) and of the final host, the eider duck Somateria mollissima. For H. elongata, and R. roscovita the distribution of their first intermediate snail hosts the periwinkle Littorina littorina has a more northern distribution. The southern occurrence of Diphterostomum brusinae and Himasthla quiessetensis could be a result of the distribution pattern of their first intermediate host Nassarius reticulatus. To the north the dogwhelk is not found on intertidal flats and as a consequence it has not been observed in north where studies of parasites in cockles have been limited to intertidal areas or lagoons without N. reticulatus. Besides this, H. quissetensis may have been overlooked in the older records as it was not registered along the east Atlantic shoreline before 1990 (Russell-Pinto, Reference Russell-Pinto1993), unless it is an introduced parasite species (de Montaudouin et al., Reference de Montaudouin, Jensen, Desclaux, Wegeberg and Sajus2005). For final hosts, generally we can expect bird hosted parasites to be more widespread than fish hosted parasites considering that many waterbirds have longer annual migratory routes than fish. As an example the fish Dicentrarchus labrax host to Bucephalus minimus has expanded its northern boundary to the North Sea probably caused by increased sea temperature. In accordance Bucephalus minimus has now been registered in the German Wadden Sea (Thieltges et al., Reference Thieltges, Krakau, Andresen, Fottner and Reise2006, Reference Thieltges, Hussel, Hermann, Jensen, Krakau, Taraschewski and Reise2008).

Compared to other bivalves co-occurring with cockles within intertidal flat communities the parasite fauna in cockles is particularly diverse and abundant (de Montaudouin et al., Reference de Montaudouin, Kisielewski, Bachelet and Desclaux2000; Thieltges & Reise, Reference Thieltges and Reise2006). Many of the parasites using cockles as second intermediate host may also be found in other bivalves (de Montaudouin et al., Reference de Montaudouin, Kisielewski, Bachelet and Desclaux2000; Krakau et al., Reference Krakau, Thieltges and Reise2006; Thieltges et al., Reference Thieltges, Krakau, Andresen, Fottner and Reise2006), whereas those using cockles as their first intermediate host are more host specific. The relatively large biogeographical area of cockles compared to some of the other bivalves from shallow water ecosystems along the east Atlantic shoreline could contribute to the richness of the supracommunity of digeneans in cockles. In addition cockles occur at a range of habitats within an ecosystem resulting in overlap with many potential first intermediate hosts (Hydrobia, Littorina and Scrobicularia). With an analogy to diversity promoters among free-living organisms, the heterogeneity of appropriate tissue types (i.e. microhabitat) is important for digenean diversity in bivalves. To what extent cockles are unique in this respect remains unresolved.

Parasites are potentially important for the dynamics of cockle populations along its entire distributional range in the north-eastern Atlantic and not just a local phenomenon. Digeneans utilizing cockles as first intermediate hosts are known to castrate their hosts and to be involved in cockle mass mortalities when additional stressors are present (Jonsson & André, Reference Jonsson and André1992; Thieltges, Reference Thieltges2006). Digeneans utilizing cockles as second intermediate host show a range of different effects such as impaired burrowing ability, reduced growth, increased mortality, and reduced tolerance of anoxia (Lauckner, Reference Lauckner and Kinne1983; Jensen et al., Reference Jensen, Fernández Castro and Bachelet1999; Wegeberg & Jensen, Reference Wegeberg and Jensen1999, Reference Wegeberg and Jensen2003). Hence, studies on cockle populations should include parasites and our identification key will hopefully facilitate inclusion of parasites in future population studies of cockles.

An understanding of the prevalence and abundance patterns requires consideration of a range of local abiotic and biotic factors determining transmission rates such as adverse environmental conditions, distance to and densities of hosts emitting parasite propagules, duration of the transmission window, age- and size-distribution of hosts, presence of ambient species interfering with the transmission of the free larval stages etc (Goater, Reference Goater1993; de Montaudouin et al., Reference de Montaudouin, Wegeberg, Jensen and Sauriau1998; Jensen et al., Reference Jensen, Fernández Castro and Bachelet1999; Wegeberg et al., Reference Wegeberg, de Montaudouin and Jensen1999; Thieltges, Reference Thieltges2007; Thieltges & Reise, Reference Thieltges and Reise2007; Thieltges, Reference Thieltges2008; Thieltges et al., in press). It will be a challenge to examine if climate-related factors or latitudinal patterns in temperature profiles have a superior impact on prevalence and abundance patterns and how global heating will impact such patterns. A clear understanding of this requires standardized experimental studies along latitudinal gradients to eliminate the importance of local factors. However, given the present knowledge of the common cockle and its parasite fauna along its latitudinal distributional area, this could be a convenient model for studying the impact of global changes on parasite–host systems.

ACKNOWLEDGEMENTS

The study was carried out with financial support from ‘Programme National Environnement Côtier’ (PNEC) and was included in the ‘Transversal Action: Impact of Parasites on Marine Organisms and populations and modulation by the environmental factors’ (TAIPAMOR), by the project 18571 CNRST (Morocco)–CNRS (France), and by the Agence Nationale de la Recherche (Project Multistress). D.W.T. acknowledges support by a fellowship from the Deutsche Forschungsgemeinschaft (DFG) (Th 1361/1-1). We are grateful to the referees for their constructive comments.

References

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Figure 0

Fig. 1. Locations from where we found data on parasites in cockles Cerastoderma edule.

Figure 1

Table 1. List of digenean species utilizing the cockle Cerastoderma edule as their first and/or second intermediate host, other hosts of the life cycle, and references to papers describing their anatomy.

Figure 2

Fig. 2. Photographs of digenean larvae as they can be observed through a dissection microscope with transmitted light, within cockle tissues squeezed between two glass slides.

Figure 3

Fig. 3. In situ location of the parasites infecting Cerastoderma edule. When mature, Gymnophallus choledochus, Bucephalus minimus and Monorchis parvus can invade most tissues.

Figure 4

Fig. 4. [See next page for Figure 4] Distribution of digenean species along the distribution of their cockle Cerastoderma edule host, in the north-eastern Atlantic. P, maximum mean parasite prevalence observed; A, maximum mean parasite abundance observed. Numbers correspond to the following references: 1. Pelseneer, 1906; 2. Vaullegard, 1894; 3. Lebour, 1911; 4. James & Bowers, 1967; 5. James et al., 1977; 6. Bowers, 1969; 7. Deltreil & His, 1972; 8. Desclaux et al., 2002; 9. Baudrimont et al., 2006; 10. Sauriau, 1992; 11. de Montaudouin et al., 2000; 12. Russell-Pinto et al., 2006; 13. Thieltges & Reise, 2006; 14. Gam et al., 2008; 15. de Montaudouin, unpublished; 16. Hancock & Urquart, 1965; 17. Boyden, 1971; 18. Malek, 2001; 19. Sannia & James, 1978; 20. Sannia et al., 1978; 21. Jonsson & André, 1992; 22. Thieltges et al., 2006; 23. Thieltges, 2006; 24. Lauckner, 1971; 25. Jonstone, 1904 (in Lebour, 1911); 26. Bowers & James, 1967; 27. Bowers et al., 1990; 28. Goater, 1993; 29. Krakau et al., 2006; 30. Lauckner, 1984; 31. Russell-Pinto, 1990; 32. Russell-Pinto & Bartoli, 1992; 33. Desclaux et al., 2004; 34. Wegeberg & Jensen, 1999; 35. Wegeberg & Jensen, 2003; 36. de Montaudouin et al., 2005; 37. Desclaux et al., 2006; 38. Kesting et al., 1996; 39. Loos-Frank, 1971; 40. Loos-Frank, 1969; 41. Thieltges & Reise, 2007; 42. Lassalle et al., 2007; 43. Goater, 1995; 44. Reimer, 1970; 45. Bazairi, unpublished; 46. Dang, unpublished 47. Bartoli et al., 2000; 48. Krakau, unpublished; 49. Jensen, unpublished.