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Type: Article
Published: 2019-12-17
Page range: 459–494
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Guide to the trematodes (Platyhelminthes) that infect the California horn snail (Cerithideopsis californica: Potamididae: Gastropoda) as first intermediate host

Scripps Institution of Oceanography-Marine Biology Research Division, University of California San Diego, La Jolla, CA 92093-0202, USA.
Platyhelminthes Cerithidea californica parasites parasitic castrators Trematoda Digenea biodiversity estuary Baja California indicators

Abstract

The California horn snail, Cerithideopsis californica, lives in estuarine habitats from California (USA) in North America to Piura (Peru) in South America. Throughout this range, the snail serves as first intermediate host for a diverse guild of digenean trematodes. These parasites are used in teaching laboratories, and have been subject to a large amount of taxonomic, biological, evolutionary, and ecological research. Despite the abundance of research on these trematodes, we lack a satisfactory guide to these parasites. This manuscript treats the 19 trematode species that we are currently able to distinguish morphologically. I provide taxonomic affinities, information on second intermediate host use, an identification key focused on cercaria traits, information and a key for regressed infections lacking cercariae, information on early infections, and species accounts. The species accounts present photographs, additional diagnostic information, taxonomic notes, information concerning cryptic species, and connections to relevant literature. The primary aim of this manuscript is to facilitate research on this trematode guild by serving as an identification tool, and by providing background information, including highlighting gaps in our knowledge.

 

References

  1. Adams, J.E. & Martin, W.E. (1963) Life cycle of Himasthla rhigedana Dietz, 1909 (Trematoda: Echinostomatidae). Transactions of the American Microscopical Society, 82, 1–6.

    https://doi.org/10.2307/3223814

    Beuret, J. & Pearson, J.C. (1994) Description of a new zygocercous cercaria (Opisthorchioidea: Heterophyidae) from prosobranch gastropods collected at Heron Island (Great Barrier Reef, Australia) and a review of zygocercariae. Systematic Parasitology, 27, 105–125.

    https://doi.org/10.1007/BF00012269

    Bils, R.F. & Martin, W.E. (1966) Fine Structure and Development of the Trematode Integument. Transactions of the American Microscopical Society, 85, 78–88.

    https://doi.org/10.2307/3224777

    Bray, R.A., Gibson, D.I. & Jones, A. (2008) Keys to the Trematoda. CAB International and the Natural History Museum, Wallingford and New York, 824 pp.

    Buck, J.C., Hechinger, R.F., Wood, A.C., Stewart, T.E., Kuris, A.M. & Lafferty, K.D. (2017) Host density increases parasite recruitment but decreases host risk in a snail-trematode system. Ecology, 98, 2029–2038.

    https://doi.org/10.1002/ecy.1905

    Deblock, S. (1966) Sur deux especes d’Echinostomes Himasthlinae (Trematodes) de Charadriiformes. Description d’ Aporchis mozambiquus n. sp. Memoires du Museum national dhistoire naturelle, Serie A, Zoologie, 41, 127–134.

    Dronen, N.O. & Blend, C.K. (2008) Observations on the Parorchis acanthus complex (Philophthalmidae : Parorchiinae) with the description of three new species of Parorchis Nicoll, 1907 and the replacement of the preoccupied junior homonym Paratrema Dronen & Badley, 1979 with Stenomesotrema nomen novum. Zootaxa, 1843 (1), 1–23.

    https://doi.org/10.11646/zootaxa.1843.1.1

    Fingerut, J.T., Zimmer, C.A. & Zimmer, R.K. (2003a) Larval swimming overpowers turbulent mixing and facilitates transmission of a marine parasite. Ecology, 84, 2502–2515.

    https://doi.org/10.1890/02-4035

    Fingerut, J.T., Zimmer, C.A. & Zimmer, R.K. (2003b) Patterns and processes of larval emergence in an estuarine parasite system. Biological Bulletin, 205, 110–120.

    https://doi.org/10.2307/1543232

    Galaktionov, K.V. & Dobrovolskij, A.A. (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 and Boston, 620 pp.

    Garcia-Vedrenne, A.E., Quintana, A.C.E., DeRogatis, A.M., Dover, C.M., Lopez, M., Kuris, A.M. & Hechinger, R.F. (2017) Trematodes with a reproductive division of labour: heterophyids also have a soldier caste and early infections reveal how colonies become structured. International Journal for Parasitology, 47, 41–50.

    https://doi.org/10.1016/j.ijpara.2016.10.003

    Garcia-Vedrenne, A.E., Quintana, A.C.E., DeRogatis, A.M., Martyn, K., Kuris, A.M. & Hechinger, R.F. (2016) Social Organization in Parasitic Flatworms—Four Additional Echinostomoid Trematodes Have a Soldier Caste and One Does Not. Journal of Parasitology, 102, 11–20.

    https://doi.org/10.1645/15-853

    Gibson, D.I., Jones, A. & Bray, R.A. (2002) Keys to the Trematoda. CAB International and the Natural History Museum, Wallingford and New York, 521 pp.

    Hechinger, R.F. (2010) Mortality affects adaptive allocation to growth and reproduction: field evidence from a guild of body snatchers. BMC Evolutionary Biology, 10 (136), 1–14.

    https://doi.org/10.1186/1471-2148-10-136

    Hechinger, R.F. & Lafferty, K.D. (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society: Biological Sciences, 272, 1059–1066.

    https://doi.org/10.1098/rspb.2005.3070

    Hechinger, R.F., Lafferty, K.D., Huspeni, T.C., Brooks, A. & Kuris, A.M. (2007) Can parasites be indicators of free-living diversity? Relationships between the species richness and abundance of larval trematodes with that of local fishes and benthos. Oecologia, 151, 82–92.

    https://doi.org/10.1007/s00442-006-0568-z

    Hechinger, R.F., Lafferty, K.D. & Kuris, A.M. (2008) Diversity increases biomass production for trematode parasites in snails. Proceedings of the Royal Society: Biological sciences, 275, 2707–2714.

    https://doi.org/10.1098/rspb.2008.0875

    Hechinger, R.F., Lafferty, K.D., Mancini III, F.T., Warner, R.R. & Kuris, A.M. (2009) How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology, 23, 651–667.

    https://doi.org/10.1007/s10682-008-9262-4

    Hechinger, R.F., Lafferty, K.D., McLaughlin, J.P., Fredensborg, B.L., Huspeni, T.C., Lorda, J., Sandhu, P.K., Shaw, J.C., Torchin, M.E., Whitney, K.L. & Kuris, A.M. (2011a) Food webs including parasites, biomass, body sizes, and life stages, for three California/Baja California estuaries. Ecology, 92, 791–791. [data paper]

    https://doi.org/10.1890/10-1383.1

    Hechinger, R.F. & Miura, O. (2014) Two ‘new’ renicolid trematodes (Trematoda: Digenea: Renicolidae) from the California horn snail, Cerithidea californica (Haldeman, 1840) (Gastropoda: Potamididae). Zootaxa, 3784 (5), 559–574.

    https://doi.org/10.11646/zootaxa.3784.5.5

    Hechinger, R.F., Wood, A.C. & Kuris, A.M. (2011b) Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proceedings of the Royal Society: Biological sciences, 278, 656–665.

    https://doi.org/10.1098/rspb.2010.1753

    Hunter, W.S. (1942) Studies on cercariae of the common mud-flat snail, Cerithidea californica. University of California, Los Angeles, 128 pp.

    Huspeni, T.C. (2000) A molecular genetic analysis of host specificity, continental geography, and recruitment dynamics of a larval trematode in a salt marsh snail. University of California, Santa Barbara, Santa Barbara, 145 pp.

    Huspeni, T.C. & Lafferty, K.D. (2004) Using larval trematodes that parasitize snails to evaluate a salt-marsh restoration project. Ecological Applications, 14, 795–804.

    https://doi.org/10.1890/01-5346

    Jones, A., Bray, R.A. & Gibson, D.I. (2005) Keys to the Trematoda. Wallingford, UK; New York, NY, USA, CAB International and the Natural History Museum, 745 pp.

    Keen, A.M. (1971) Sea shells of tropical West America marine mollusks from Baja California to Peru. Stanford University Press, Stanford, 1064 pp.

    Koprivnikar, J., Lim, D., Fu, C. & Brack, S.H.M. (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research, 106, 1167–1177.

    https://doi.org/10.1007/s00436-010-1779-0

    Kuris, A.M. (1990) Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In: Esch, G.W., Bush, A.O. & Aho, J.M. (Eds.) Parasite communities: patterns and processes. Chapman and Hall, London, pp. 69–100.

    https://doi.org/10.1007/978-94-009-0837-6_4

    Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., Dobson, A.P., Dunham, E.J., Fredensborg, B.L., Huspeni, T.C., Lorda, J., Mababa, L., Mancini, F.T., Mora, A.B., Pickering, M., Talhouk, N.L., Torchin, M.E. & Lafferty, K.D. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454, 515–518.

    https://doi.org/10.1038/nature06970

    Lafferty, K.D. (1993a) Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Marine Ecology Progress Series, 96, 229–237.

    https://doi.org/10.3354/meps096229

    Lafferty, K.D. (1993b) The marine snail, Cerithidea californica, matures at smaller sizes where parasitism is high. Oikos, 68, 3–11.

    https://doi.org/10.2307/3545303

    Lafferty, K.D. & Kuris, A.M. (2009) Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 364, 1659–1663.

    https://doi.org/10.1098/rstb.2008.0220

    Lafferty, K.D. & Morris, A.K. (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology, 77, 1390–1397.

    https://doi.org/10.2307/2265536

    Lafferty, K.D., Sammond, D.T. & Kuris, A.M. (1994) Analysis of larval trematode communities. Ecology, 75, 2275–2285.

    https://doi.org/10.2307/1940883

    Lafuente, M., Roca, V. & Carbonell, E. (2000) Description of Acanthotrema armata n. sp. (Trematoda: Heterophyidae) from Larus audouinii (Aves: Laridae), with an amended diagnosis of the genus Acanthotrema Travassos, 1928. Systematic Parasitology, 45, 131–134.

    https://doi.org/10.1023/A:1006293611598

    LeFlore, W.B., Bass, H.S. & Martin, W.E. (1985) The life cycle of Cloacitrema michiganensis McIntosh, 1938 (Trematoda: Philophthalmidae). The Journal of Parasitology, 71, 28–32.

    https://doi.org/10.2307/3281973

    Martin, W.E. (1950a) Euhaplorchis californiensis n.g., n.sp., Heterophyidae, Trematoda, with notes on its life cycle. Transactions of the American Microscopical Society, 194–209.

    https://doi.org/10.2307/3223410

    Martin, W.E. (1950b) Parastictodora hancocki n. gen., n. sp. (Trematoda: Heterophyidae). with observations on its life cycle. Journal of Parasitology, 36, 360–370.

    https://doi.org/10.2307/3273472

    Martin, W.E. (1950c) Phocitremoides ovale n. gen., n. sp. (Trematoda: Opisthorchiidae), with observations on its life cycle. Journal of Parasitology, 36, 552–558.

    https://doi.org/10.2307/3273288

    Martin, W.E. (1951) Pygidiopsoides spindalis n. gen., n. sp., (Heterophyidae; Trematoda), and its second intermediate host. Journal of Parasitology, 37, 297–300.

    https://doi.org/10.2307/3273202

    Martin, W.E. (1955) Seasonal infections of the snail, Cerithidea californica Haldeman, with larval trematodes. In: Essays in Natural Science in Honor of Captain Alan Hancock on the occasion of his birthday. University of Southern California Press, Los Angeles, California, pp. 203–210.

    Martin, W.E. (1956) The Life Cycle of Catatropis johnstoni n. sp. (Trematoda: Notocotylidae). Transactions of the American Microscopical Society, 75, 117–128.

    https://doi.org/10.2307/3223661

    Martin, W.E. (1961) Life cycle of Mesostephanus appendiculatus (Ciurea, 1916) Lutz, 1935 (Trematoda: Cyathocotylidae). Pacific Science, 15, 278–281.

    Martin, W.E. (1964) Life cycle of Pygidiopsoides spindalis Martin, 1951 (Heterophyidae: Trematoda). Transactions of the American Microscopical Society, 83, 270–272.

    https://doi.org/10.2307/3224579

    Martin, W.E. (1971) Larval stages of renicolid trematodes. Transactions of the American Microscopical Society, 90, 188–194.

    https://doi.org/10.2307/3225025

    Martin, W.E. (1972) An annotated key to the cercariae that develop in the snail Cerithidea californica. Bulletin of the Southern California Academy of Sciences, 71, 39–43.

    Martin, W.E. & Adams, J.E. (1961) Life Cycle of Acanthoparyphium spinulosum Johnston, 1917 (Echinostomatidae: Trematoda). The Journal of Parasitology, 47, 777–782.

    https://doi.org/10.2307/3275470

    Maxon, M.G. & Pequegnat, W.E. (1949) Cercariae from upper Newport Bay. Journal of Entomology and Zoology, 41, 30–55.

    Miura, O., Torchin, M.E. & Bermingham, E. (2010) Molecular phylogenetics reveals differential divergence of coastal snails separated by the Isthmus of Panama. Molecular Phylogenetics and Evolution, 56, 40–48.

    https://doi.org/10.1016/j.ympev.2010.04.012

    Mordecai, E.A., Jaramillo, A.G., Ashford, J.E., Hechinger, R.F. & Lafferty, K.D. (2016) The role of competition–colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence. Ecology, 97, 1484–1496.

    https://doi.org/10.1890/15-0753.1

    Nadakal, A.M. (1960a) Chemical nature of cercarial eye-spot and other tissue pigments. Journal of Parasitology, 46, 475–481.

    https://doi.org/10.2307/3275140

    Nadakal, A.M. (1960b) Types and sources of pigments in certain species of larval trematodes. Journal of Parasitology, 46, 777–786.

    https://doi.org/10.2307/3275532

    Nguyen, A.T., Kuwata, C. & Kuris, A.M. (2015) A synthetic workflow for coordinated direct observation and genetic tagging applied to a complex host-parasite interaction. Parasitology Research, 114, 2015–2021.

    https://doi.org/10.1007/s00436-015-4437-8

    Oates, J. & Fingerut, J. (2011) Internal Movement of Estuarine Digenetic Trematodes Through Their Intermediate Snail Host Cerithidea californica. Journal of Parasitology, 97, 1181–1183.

    https://doi.org/10.1645/GE-2766.1

    Reid, D.G. & Claremont, M. (2014) The genus Cerithideopsis Thiele, 1929 (Gastropoda: Potamididae) in the Indo-West Pacific region. Zootaxa, 3779 (1), 61–80.

    https://doi.org/10.11646/zootaxa.3779.1.8

    Robinson, H.W. (1952) A Preliminary Report on the Life Cycle of Cloacitrema michiganensis McIntosh, 1938 (Trematoda). The Journal of Parasitology, 38, 368–368.

    https://doi.org/10.2307/3273777

    Sarkisian, L.N. (1957) Maritrema uca, new species (Trematoda: Microphallidae), from the fiddler crab, Uca crenulata (Lockington). The Wasmann Journal of Biology, 15, 35–48.

    Sousa, W.P. (1983) Host life history and the effect of parasitic castration on growth a field study of Cerithidea californica (Gastropoda: Prosobranchia) and its trematode parasites. Journal of Experimental Marine Biology and Ecology, 73, 273–296.

    https://doi.org/10.1016/0022-0981(83)90051-5

    Sousa, W.P. (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs, 63, 103–128.

    https://doi.org/10.2307/2937176

    Sousa, W.P. & Gleason, M. (1989) Does parasitic infection compromise host survival under extreme environmental conditions: the case for Cerithidea californica (Gastropoda: Prosobranchia). Oecologia, Berlin, 80, 456–464.

    https://doi.org/10.1007/BF00380066

    Tkach, V.V., Kudlai, O. & Kostadinova, A. (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology, 46, 171–185.

    https://doi.org/10.1016/j.ijpara.2015.11.001

    Torchin, M.E., Miura, O. & Hechinger, R.F. (2015) Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts Ecology, 96, 3033–3042.

    https://doi.org/10.1890/15-0518.1

    Walker, J.C. (1979) Austrobilharzia terrigalensis: A schistosome dominant in interspecific interactions in the molluscan host. International Journal for Parasitology, 9, 137–140.

    https://doi.org/10.1016/0020-7519(79)90104-8

    Weinersmith, K.L., Brown, C.E., Clingen, K.B., Jacobsen, M.C., Topper, L.B. & Hechinger, R.F. (2018) Euhaplorchis californiensis Cercariae Exhibit Positive Phototaxis and Negative Geotaxis. Journal of Parasitology, 104, 329–333.

    https://doi.org/10.1645/17-80

    Whitney, K.L., Hechinger, R.F., Kuris, A.M. & Lafferty, K.D. (2007) Endangered species and parasites: light-footed clapper rail (Rallus longirostris levipes) affects parasite community structure in coastal wetlands. Ecological Applications, 17, 1694–1702.

    https://doi.org/10.1890/06-1325.1

    Yoshino, T.P. (1975) A seasonal and histologic study of larval Digenea infecting Cerithidea californica (Gastropoda: Prosobranchia) from Goleta Slough, Santa Barbara County, California, USA. Veliger, 18, 156–161.

    Zimmer, R.K., Fingerut, J.T. & Zimmer, C.A. (2009) Dispersal pathways, seed rains, and the dynamics of larval behavior. Ecology, 90, 1933–1947.

    https://doi.org/10.1890/08-0786.1