Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Trematode maturation patterns in a migratory snail host: What happens during upshore residency in a Mediterranean lagoon?


Maturation of trematode larval stages is expected to be temporally and spatially adapted to maximise the encounter with the adequate downstream host, i.e. the host, which will be infected by this parasite stage. Since studies on intramolluscan parasite maturation are scarce but important in the context of parasite transmission, the larval development inside sporocysts was monitored during upshore residency of the snail host Gibbula adansonii (Trochidae), i.e., from March to May (2011 and 2013), when these snails temporarily reside in the intertidal habitat of a Western Mediterranean lagoon (40° 37′ 35″ N, 0° 44′ 31″ E, Spain). Data on the relative quantity of different maturation stages of Cainocreadium labracis and Macvicaria obovata (Opecoelidae) parasitising the G. adansonii as well as on snail and sporocyst size were explored using linear models and linear mixed models. The effect of the trematodes on snail growth was shown to be species-specific, with snail and sporocyst size acting as proxies of the reproductive capacity of M. obovata but not that of C. labracis. The number of cercarial embryos and germinal balls did not show monthly variation in either parasite species, but a higher number of mature stages and the highest maturity index was found in April. Hence, during the snail’s limited spawning-related presence in the upshore waters of the lagoon, continuous production and output of infectious cercariae was observed, which indicates a link between larval maturation and snail migration. The synchronization of snails, mature parasite transmission stages and downstream hosts in time and space guarantees a successful completion of the life cycle.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. Antoniadou C, Koutsoubas D, Chintiroglou CC (2005) Mollusca fauna from infralittoral hard substrate assemblages in the North Aegean Sea. Belg J Zool 135:119–126

  2. Arruda LM, Azevedo JN, Neto AI (1993) Abundance, age-structure and growth, and reproduction of Gobies (Pisces; Gobiidae) in the Ria de Aveiro Lagoon (Portugal). Estuar Coast Shelf Sci 37:509–523

  3. Averbuj A, Cremonte F (2010) Parasitic castration of Buccinanops cochlidium (Gastropoda: Nassariidae) caused by a lepocreadiid digenean in San José Gulf, Argentina. J Helminthol 84:381–389

  4. Bachelet G, Simon-Bouhet B, Desclaux C, Garcia-Meunier P, Mairesse G, de Montaudouin X, Raigné H, Randriambao K, Sauriau P-G, Viard F (2004) Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea: origin and effects on resident fauna. Mar Ecol Prog Ser 276:147–159

  5. Bao-Zhen Q, Jun Q, Dong-Mei X, Johansen MV (1997) The population dynamics of cercariae of Schistosoma japonicum in Oncomelania hupensis. Southeast Asian J Trop Med Public Health 28:296–302

  6. Barnes RSK (1980) Coastal lagoons. The natural history of a neglected habitat. Cambridge University Press, Cambridge

  7. Bartoli P, Boudouresque CF (2007) Effect of the digenean parasites of fish on the fauna of Mediterranean lagoons. Parassitologia 49:111–117

  8. Bartoli P, Gibson DI (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the Western Mediterranean. J Nat Hist 41:1553–70

  9. Bartoli P, Prévot G (1986) Stratégies d’infestation des hotes cibles chez les trématodes marins parasites de Larus cachinnans michaellis de Provence. Ann Parasitol Hum Comp 61(5):533–552

  10. Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. ArXiv e-print; submitted to Journal of Statistical Software, http://arxiv.org/abs/1406.5823

  11. Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352

  12. Beck LA (1995) Zur Systematik und Evolution europäischer Trochiden (Kreiselschnecken) unter besonderer Berücksichtigung der Gattungen Gibbula RISSO, 1826, Osilinus Philippi, 1847 und Jujubinus Monterosato, 1884 (Gastropoda, Prosobranchia). Europäische Kreiselschnecken (Trochoidea). http://www.staff.uni-marburg.de/∼beck/diss1995/. Accessed 15 June 2015

  13. Blair D, Davis GM, Wu B (2001) Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123:S229–S243

  14. Born-Torrijos A, Kostadinova A, Raga JA, Holzer AS (2012) Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitising prosobranch snails in a Western Mediterranean lagoon. Parasitol Int 61:450–460

  15. Born-Torrijos A, Holzer AS, Raga JA, Kostadinova A (2014a) Same host, same lagoon, different transmission pathways: effects of exogenous factors on larval emergence in two marine digenean parasites. Parasitol Res 113:545–554

  16. Born-Torrijos A, Poulin R, Raga JA, Holzer AS (2014b) Estimating trematode prevalence in snail hosts using a single-step duplex PCR: how badly does cercarial shedding underestimate infection rates? Parasit Vectors 7:243

  17. Bouchereau JL, Guelorget O (1998) Comparison of three Gobiidae (Teleostei) life history strategies over their geographical range. Oceanol Acta 21:503–517

  18. Byrd EE, Scofield GF (1954) Developmental Stages in the Digenea. III. Observations on the number of daughter sporocysts and cercariae produced in Physa gyrina as a result of single and multiple ochetosomatid egg-exposures. J Parasitol 40:1–21

  19. Cort WW, Ameel DJ, Van der Woude A (1954) Germinal development in the sporocysts and rediae of the digenetic trematodes. Parasitol Rev 3:185–225

  20. Crocetta F, Renda W, Vazzana A (2009) Alien mollusca along the calabrian shores of the Messina Strait area and a review of their distribution in the Italian seas. Boll Malacol 45:15–30

  21. Curtis LA (1987) Vertical distribution of an estuarine snail altered by a parasite. Science 235:1509–1511

  22. Desai BN (1966) The biology of Monodonta lineata (da Costa). Proc Malac Soc Lond 37:1–17

  23. Dobrovolskij AA, Galaktionov КV, Ataev GL (2000) Peculiarities of the generative material organization and proliferation dynamics of mother sporocyst trematodes. Parazitologiya 34:14–24 (In Russian)

  24. Elliott M, Hemingway KL (2002) Fishes in estuaries. Wiley-Blackwell, Oxford

  25. Fermer J, Culloty SC, Kelly TC, O’Riordan RM (2009) Intrapopulational distribution of Meiogymnophallus minutes (Digenea, Gymnophallidae) infections in its first and second intermediate host. Parasitol Res 105:1231–1238

  26. Fermer J, Culloty SC, Kelly TC, O’Riordan RM (2010) Temporal variation of Meiogymnophallus minutus infections in the first and second intermediate host. J Helminthol 84:362–368

  27. Fernandez J, Esch GW (1991) Effect of parasitism on the growth rate of the pulmonate snail Helisoma anceps. J Parasitol 77:937–944

  28. Fredensborg BL, Mouritsen KN, Poulin R (2006) Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail - from small to large scale. Mar Biol 149:275–283

  29. Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, The Natural History Museum, London

  30. Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands

  31. Gérard C, Moné H, Théron A (1993) Schistosoma mansoniBiomphalaria glabrata: dynamics of the sporocyst population in relation to the miracidial dose and the host size. Can J Zool 71:1880–1885

  32. Gorbushin AM, Levakin IA (1999) The effect of Trematode parthenitae on the growth of Onoba aculeus, Littorina saxatilis and L. obtusata (Gastropoda: Prosobranchia). J Mar Biol Ass UK 79:273–279

  33. Graham AL (2003) Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. J Parasitol 89:458–463

  34. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363, http://cran.r-project.org/web/packages/multcomp/

  35. Hughes RN, Answer P (1982) Growth, spawning and trematode infections of Littorina littorea (L.) from an exposed shore in North Wales. J Mollus Stud 48:321–330

  36. Karvonen A, Savolainen M, Seppälä O, Valtonen ET (2006) Dynamics of Diplostomum spathaceum infection in snail hosts at a fish farm. Parasitol Res 99:341–345

  37. Kendall MA, Williamson P, Garwood PR (1987) Annual variation in recruitment and population structure of Monodonta lineata and Gibbula umbilicalis populations at Aberaeron, Mid-Wales. Estuar Coast Shelf Sci 24:499–511

  38. Koutsoubas D, Arvanitidis C, Dounas C, Drummond L (2000) Community structure and dynamics of the Molluscan Fauna in a Mediterranean lagoon (Gialova lagoon, SW Greece). Belg J Zool 130:131–138

  39. Korniychuk YM (2008) Parthenogenetic generations of Helicometra fasciata Rud., 1819 (Trematoda: Opecoelidae) in the Black Sea molluscs Gibbula adriatica. Parazitologiya 42:41–52 (In Russian)

  40. Kube S, Kube J, Bick A (2002) Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variations in prevalence in relation to host life history. J Parasitol 88:730–737

  41. Lang WH, Dennis EA (1976) Morphology and seasonal incidence of infection of Proctoeces maculatus (Looss, 1901) Odhner, 1911 (Trematoda) in Mytilus edulis L. Ophelia 15:65–75

  42. Lauckner G (1980) Diseases of mollusca: Gastropoda. In: Kinne O (ed) Diseases of marine animals, vol I, General aspects. Protozoa to Gastropoda. John Wiley and Sons, New York, pp 311–424

  43. Lie KJ (1969) Role of immature rediae in antagonism of Paryphostomum segregatum to Schistosoma mansoni and larval development in degenerated sporocysts. Z Parasitenk 32:316–323

  44. Loker ES (1983) A comparative study of the life-histories of mammalian schistosomes. Parasitology 87:343–369

  45. Maillard C (1971) Developmental cycle of Cainocreadium labracis (Dujardin, 1845) (Trematoda, Allocreadiidae). C R Acad Sci Paris, Sér D 272:3303–3306

  46. McCarthy HO, Fitzpatrick S, Irwin SWB (2002) Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics. J Parasitol 88(5):910–918

  47. McCarthy HO, Fitzpatrick S, Irwin SWB (2004) Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages. Parasitology 128:7–14

  48. McCurdy DG, Boates JS, Forbes MR (2000) Spatial distribution of the intertidal snail Ilyanassa obsoleta in relation to parasitism by two species of trematodes. Can J Zool 78:1137–1143

  49. Milazzo M, Chemello R, Badalamenti F, Riggio S (2000) Molluscan assemblages associated with photophilic algae in the Marine Reserve of Ustica Island (Lower Tyrrhenian Sea, Italy). Ital J Zool 67:287–295

  50. Miura O, Chiba S (2007) Effects of trematode double infection on the shell size and distribution of snail hosts. Parasitol Int 56:19–22

  51. Muñoz G, Torres P, Valdés J, Rodríguez A (2013) Spatio-temporal variation in the prevalence of trematodes in the bivalve Perumytilus purpuratus. Acta Parasitol 58:155–166

  52. Palacín C, Martin D, Gili JM (1991) Features of spatial distribution of benthic infauna in a Mediterranean shallow-water bay. Mar Biol 110:315–321

  53. Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299

  54. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

  55. Prinz K, Kelly TC, O’Riordan RM, Culloty SC (2010) Temporal variation in prevalence and cercarial development of Echinostephilla patellae (Digenea, Philophthalmidae) in the intertidal gastropod Patella vulgate. Acta Parasitol 55:39–44

  56. Probst S, Kube J (1999) Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia ventrosa (Gastropoda: Prosobranchia)? J Exp Mar Biol Ecol 238:49–68

  57. R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org

  58. Rakotondravao MA, Hourdin P, Rondelaud D (1992) Redial generations of Fasciola gigantica in the pulmonate snail Lymnaea truncatula. J Helminthol 66:159–166

  59. Ribeiro J, Carvalho GM, Gonçalves JMS, Erzini K (2012) Fish assemblages of shallow intertidal habitats of the Ria Formosa lagoon (South Portugal): influence of habitat and season. Mar Ecol Prog Ser 446:259–273

  60. Rondelaud D, Barthe D (1987) Fasciola hepatica L.: etude de la productivité d'un sporocyste en fonction de la taille de Lymnaea truncatula Müller. Parasitol Res 74:155–160

  61. Soppelsa O, Crocetta F, Fasulo G (2007) I molluschi marini di Punta di Pioppeto (Isola di Procida—Campania). Boll Malacol 43:21–32

  62. Sousa WP (1983) Host life history and the effect of parasitic castration on growth: a field study of Cerithidea caffornica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. J Exp Mar Biol Ecol 13:273–296

  63. Thieltges DW (2007) Habitat and transmission - effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve. Parasitology 134:599–605

  64. Thieltges DW, Jensen KT, Poulin R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426

  65. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:137–151

  66. Touassem R, Théron A (1986) Study on the intramolluscal development of Schistosoma bovis: demonstration of three patterns of sporocystogenesis by daughter sporocysts. Parasitology 92:337–341

  67. Underwood AJ (1973) Studies on zonation of intertidal prosobranch molluscs in the Plymouth Region. J Anim Ecol 42:353–372

  68. Williams EE (1965) The growth and distribution of Monodonta lineata (da Costa) on a rocky shore in Wales. Field Stud 2:189–198

Download references


The authors highly acknowledge the help of Tsukushi Kamiya for the design and adjustment of the statistical models, and Gabrielle S. van Beest for the help with snail measurements. This research was supported by the following projects: Prometeo/2015/018 and Revidpaqua ISIC/2012/003 funded by the Local Valencian Government (JAR), CGL2011-30413 project funded by the Spanish Ministry of Science and Innovation (AB-T) and by the European Centre of Ichtyoparasitology (grant 505/12/G112, Center of Excellence) funded by the Czech Science Foundation, (ASH). AB-T is the recipient of a doctoral fellowship (Ministry of Education and Science, Spain; grant AP2009-2560).

Author information

Correspondence to Ana Born-Torrijos.

Electronic supplementary material

Below is the link to the electronic supplementary material.


(PDF 536 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Born-Torrijos, A., Raga, J.A. & Holzer, A.S. Trematode maturation patterns in a migratory snail host: What happens during upshore residency in a Mediterranean lagoon?. Parasitol Res 115, 575–585 (2016). https://doi.org/10.1007/s00436-015-4774-7

Download citation


  • Larval maturation
  • Snail migration
  • Trematodes
  • Cainocreadium labracis
  • Macvicaria obovata
  • Mediterranean lagoon