Ecological Archives E089-064-A3

April M. H. Blakeslee and James E. Byers. 2008. Using parasites to inform ecological history: comparisons among three congeneric marine snails. Ecology 89:1068–1078.

Appendix C. Trematode taxonomy operational procedures for Table 1 prevalence data.

When assessing the overall data presented in Table 1, there are some taxonomic issues that might affect our reported prevalence for certain trematode species. In addition, for some of the species we report, questions have been raised in the literature regarding their distinctions as separate species. Due to the taxonomic issues described in the species below, their prevalences as reported in the Literature columns of Table 1 may not accurately reflect their true prevalences in nature because species identifications were not standard across all studies in the literature. The most notable of these issues are described below.

First, two trematode species, Cercaria parvicaudata and Renicola roscovita, are typically distinguished based on the color of their sporocysts, which are "orange" for Cercaria parvicaudata and "cream" for R. roscovita (James 1968a, Stunkard 1971); this can obviously be highly subjective (Galaktionov and Skirnisson 2000). Furthermore, these two species have been debated in the literature as to their status as separate species (e.g., Stunkard 1950, Galaktionov and Skirnisson 2000), and some authors have lumped them as Renicola spp. (e.g., Granovitch et al. 2000), referred to Cercaria parvicaudata as Renicola parvicaudata (Lauckner 1980), or described Cercaria parvicaudata as a synonym of R. roscovita (Pohley 1976). For our study, we have used James’s Littorina sp. trematode taxonomic key (1968a)—primarily the distinction based upon sporocyst color—in order to distinguish the two species, which Stunkard (1950) reported as the only distinct characteristic: "except for the difference in color of the sporocysts, the two species [Cercaria parvicaudata and R. roscovita] are almost identical." However, color distinctions are subjective and may not remain universal from researcher to researcher, but because we have used this technique for distinguishing species across populations in our field surveys and because Cercaria parvicaudata and Renicola roscovita have been described in Europe and North America in both the field and literature, it should have little affect on our overall species richness counts and comparisons between the regions.

Second, the two Himasthla species, H. elongata and H. littorinae, can also be difficult to distinguish morphologically (Galaktionov and Skirnisson 2000) and have sometimes been lumped in the literature as Himasthla spp. (e.g., Matthews et al. 1985, Galaktionov and Bustnes 1995, Mouritsen et al. 1999). For our study, we have distinguished these species using James' Littorina sp. trematode taxonomic key (1968a) and descriptions by Stunkard (1966, 1983). In James' key, H. elongata was reported as H. leptosoma, which was a misidentification. H. leptosoma is a different species and uses the snail, Hydrobia ulvae, as its first-intermediate host (Galaktionov and Skirnisson 2000). Therefore, what James (1968a) reported as H. leptosoma in his key is actually the species H. elongata, and we have used this key in distinguishing H. elongata and H. littorinae.

Second, the "pygmaeus" microphallid group is a group of four species (Microphallus pirifomis, M. pygmaeus, M. pseudopygmaeus, and M. triangulatus) that are morphologically similar due to their close phylogenetic relationships (Galaktionov et al. 2004) and also due to their infection life cycle, which uses the snail as both a first- and second-intermediate host. When the microphallid species metacercariae mature within their snail hosts (Galaktionov et al. 2004), they often become difficult to distinguish to species level, and there is still debate regarding the morphological differentiation of some of these microphallid species (Galaktionov and Skirnisson 2000) though recent molecular evidence has shown M. piriformis and M. pygmaeus to be genetically distinct while M. pseudopygmaeus and M. triangulatus form a species complex (Galaktionov et al. 2004). In our investigations, we primarily observed these trematodes in their metacercarial state (we only observed cercariae on one or two occasions); and therefore, we could not be confident in distinguishing the four microphallids of the "pygmaeus" group and so have lumped them in both Europe and North America. In the literature, these four microphallids have also been lumped either as Microphallus spp. or as microphallids of the “pygmaeus” group (Granovitch 1992, Galaktionov and Bustnes 1995, Saville et al. 1997, Galaktionov and Skirnisson 2000) and prior to the understanding that the “pygmaeus” group was four species, they were described just as Microphallus pygmaeus (the initially described microphallid (Galaktionov and Skirnisson 2000)). In sum, the highly similar morphological details of these trematode species make it very unlikely that authors throughout the years would have applied a consistent standard to differentiate these species correctly, which is why we have chosen to lump the species in our investigation.

Overall, we are confident in our species identifications, barring these individual cases described above where there has been debate or ambiguousness in the literature. In such cases, we have relied on morphological characters found across sources or in the case of the "pygmaeus" group of species, we have lumped them for reasons described in the previous section. As we have applied these criteria in both Europe and North America, there should be little effect on overall trematode species richness counts and comparisons between the regions and therefore should not greatly impact our conclusions based upon the patterns we observed in species richness between the regions.


Galaktionov, K., and J. Bustnes. 1995. Species composition and prevalence of seabird trematode larvae in periwinkles at two littoral sites in North-Norway. Sarsia 80:187–191.

Galaktionov, K., and K. Skirnisson. 2000. Digeneans from intertidal molluscs of SW Ireland. Systematic Parasitology 47:87–101.

Galaktionov, K., S. A. Bulat, I. A. Alekhina, D. H. Saville, S. M. Fitzpatrick, and S. W. B. Irwin. 2004. An investigation of evolutionary relationships within "pygmaeus" group microphallids (Trematoda: Microphallidae) using genetic analysis and scanning electron microscopy. Journal of Helminthology 78: 231–236.

Granovitch, A. 1992. The effect of trematode infection on the population structure of Littorina saxatilis (Olivi) in the White Sea. Pages 255-263 in J. Grahame, P. Mill, D. Reid, editors. Proceedings of the Third International Symposium on Littorinid Biology. The Malacological Society of London, London, UK.

Granovitch, A., S. Sergievsky, and I. Sokolova. 2000. Spatial and temporal variation of trematode infection in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Diseases of Aquatic Organisms 41:53–64.

James, B. 1968a. The distribution and keys of species in the family Littorinidae and of their digenean parasites, in the region of Dale, Pembrokeshire. Field Studies 2: 615–650.

James, B. 1969. The Digenea of the intertidal prosobranch, Littorina saxatilis (Olivi). Z. Zool. Syst. Evol. Fursch 7:273–316.

Lauckner, G. 1980. Diseases of Mollusca: Gastropoda. Pages 311–424 in O. Kinne, editor. Diseases of Marine Animals. Biologische Anstalt Helgoland, Hamburg, Germany.

Lauckner, G. 1985. 3. Diseases of Aves (Marine Birds). Pages 627–637 in O. Kinne, editor. Diseases of Marine Animals. Biologische Anstalt Helgoland, Hamburg, Federal Republic of Germany.

Matthews, P., W. Montgomery, and R. Hanna. 1985. Infestation of littorinids by larval Digenea around a small fishing port. Parasitology 90:277–287.

Mouritsen, K., A. Gorbushin, and K. Jensen. 1999. Influence of trematode infections on in situ growth rates of Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 79:425–430.

Pohley, W. 1976. Relationships among three species of Littorina and their larval Digenea. Marine Biology 37:179–186.

Sannia, A., and B. James. 1977. The Digenea in marine molluscs from Eyjafjordur, North Iceland. Ophelia 16:97–109.

Saville, D., K. Galaktionov, S. Irwin, and I. Malkova. 1997. Morphological comparison and identification of metacercariae in the 'pygmaeus' group of microphallids, parasites of seabirds in western palaearctic regions. Journal of Helminthology 71:167–174.

Stunkard, H. 1950. Further observations on Cercariae parvicaudata Stunkard and Shaw, 1931. Biological Bulletin 99:136–142.

Stunkard, H. 1966. The morphology and life history of the digenetic trematode, Himasthla littorinae sp. n. (Echinostomatidae). Journal of Parasitology 52:367–372.

Stunkard, H. 1971. Revue critique renicolid trematodes (Digenea) from the renal tubules of birds. Annales de Parasitologie (Paris) 46:109–118.

Stunkard, H. 1983. The marine cercariae of the Woods Hole, Massachusetts region, a review and a revision. Biological Bulletin 164:143–162.

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