Ecological Archives A014-016-A1

Todd C. Huspeni and Kevin D. Lafferty. 2004. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 14:795–804.

Appendix A. Life cycles and hosts used by larval trematodes infecting Cerithidea californica.

Trematode species infecting Cerithidea californica

Type of second intermediate host

Commonly observed second intermediate host species

Reported definitive host species

Acanthoparyphium spinulosum [1]

Molluscs and polychaetes

Gastropods:

   Cerithidea californica [1]

    Melampus olivaceus [2]

Bivalves:

   Chione spp. [3]

   Tagelus spp. [4]

Nereid polychaetes [3, 5]

American Oystercatcher [6]

American Avocet [7]

Black-bellied Plover [7]

Short-billed Dowitcher [7]

Western Sandpiper [7]

Least Sandpiper [7]

Catatropis johnstoni [8]

Hard substrates

Gastropods:

   Cerithidea californica [2]

Crustaceans:

   Hemigrapsus oregonensis [4]

   Pachygrapsus crassipes [4]

American Avocet [7]

Black-bellied Plover [7]

Willet [7]

Dunlin [7]

Western Sandpiper [7]

Rice Rat (Oryzomys palustris) [9]

Cloacitrema michiganensis [10, 11]

Hard substrates

Gastropods:

   Cerithidea californica [12]

Bivalves:

   Tagelus spp. [3]

Black-bellied Plover [7]

Marbled Godwit [7]

Willet [10]

Short-billed Dowitcher [7]

Dunlin [7]

Western Sandpiper [7]

Least Sandpiper [7]

California Gull [7]

Euhaplorchis californiensis [13]

Fish

   Fundulus parvipinnis [13]

American Avocet [7]

Himasthla sp. B [5, 14]

Molluscs

Gastropods:

   Acteocina inculta [12]

   Cerithidea californica (< 10mm)   [12]

Short-billed Dowitcher [15]

Spotted Sandpiper

Himasthla rhigedana [16]

Hard substrates

Gastropods:

   Cerithidea californica [4]

Crustaceans:

   Hemigrapsus oregonensis [4]

   Pachygrapsus crassipes [4]

   Uca spp. [3]

   Neotrypaea californiensis [3]

Long-billed Curlew [17]

Willet [7]

Spotted Sandpiper

Large xiphidiocercaria [5]

Molluscs§

Unknown

Unknown

Mesostephanus appendiculatus [18]

Fishes

   Fundulus parvipinnis [18]

   Gillichthys mirabilis [19]

   Clevelandia ios [19]

Unknown

Parorchis spp. [14, 20, 21]

Hard substrates

Gastropods:

   Cerithidea californica [12]

Bivalves:

   Tagelus spp. [3]

Crustaceans:

   Hemigrapsus oregonensis [4]

Marbled Godwit [7]

Long-billed Curlew [17]

Willet [7]

Short-billed Dowitcher [7]

Herring Gull [21]

Dunlin [7]

Western Sandpiper [7]

Least Sandpiper [7]

Phocitremoides ovale [22]

Fishes

   Fundulus parvipinnis [22]

   Atherinops affinis [22]

Unknown

Probolocoryphe uca [5, 23]

Crustaceans

   Hemigrapsus oregonensis [4]

   Pachygrapsus oregonensis [3]

   Uca spp. [3, 23]

Willet [4]

Pygidiopsoides spindalis [24]

Fishes

   Fundulus parvipinnis [24]

   Gillichthys mirabilis [25]

   Clevelandia ios [26]

Unknown

Renicola buchanani [27, 28]

Fishes

   Fundulus parvipinnis [28]

   Gillichthys mirabilis [19]

Short-billed Dowitcher [7]

Dunlin [7]

Least Sandpiper [7]

California Gull [5]

Renicola cerithidicola [28]

Fishes

   Fundulus parvipinnis [28]

   Gillichthys mirabilis [26]

Short-billed Dowitcher [7]

Dunlin [7]

California Gull [5]

Least Sandpiper [7]

Small cyathocotylid [5]

Fishes

   Fundulus parvipinnis [5]

   Gillichthys mirabilis [26]

   Clevelandia ios [26]

   Atherinops affinis [26]

Unknown

 Euhaplorchis californiensis has only been found in significant intensities the brain of Fundulus parvipinnis, despite extensive searches in Gillichthys mirabilis, Clevelandia ios, and Atherinops affinis.

 The species referred to here as Himasthla species B was referred to as Echinoparyphium sp. in Martin’s 1972 key and elsewhere in the ecological literature.  Careful examination of collar spine morphology and life cycle characteristics indicates this species belongs in the genus Himasthla, and is referred to here as Himasthla sp. B.

§ Martin (1972) refers to this species as a microphallid.  Microphallids typically use crustaceans as second intermediate hosts.  However, the morphology of the cercaria of this species indicates that it is a type of renicolid that uses molluscs as second intermediate hosts.

Sources:

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

2. T. Huspeni and R. Hechinger, unpublished data.

3. R. Hechinger, unpublished data.

4. Stevens, T.  1996.  The importance of spatial heterogeneity in organisms with complex life cycles: analysis of digenean trematodes in a salt marsh community.  Dissertation.  University of California, Santa Barbara, California, USA.

5. 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.

6. Dronen, N. O., G. D. Schmidt, B. R. Allison, and J. W. Mellen.  1988.  Some parasitic helminthes from the American Oystercatcher, Haematopus palliates, Temminck from the Texas Gulf coast and the Common Pied Oystercatcher, Haematopus ostralegus Linnaeus from New Zealand including Dildotaenia latovarium, new genus, new species (Cestoda: Hymenolepididae).  Journal of Parasitology  74:864–867.

7. Russell, H. T.  1960.  Trematodes from shorebirds collected at Morro Bay, California.  Dissertation.  University of California, Los Angeles, California, USA.

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

9. Bush, A. O., and J. M. Kinsella.  1972.  A natural definitive host for Catatropis johnstoni Martin, 1956 (Trematoda: Notocotylidae), with notes on experimental host specificity and intraspecific variation.  Journal of Parasitology 58:843–845.

10. Robinson, H. W.  1952.  A preliminary report of the life cycle of Cloacitrema michiganensis McIntosh, 1938 (Trematoda).  Journal of Parasitology 38:368.

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

12. T. Huspeni, unpublished data.

13. Martin, W. E.  1950.  Euhaplorchis californiensis n.g., n.sp., Heterophyidae, Trematoda, with notes on its life cycle.  Transactions of the American Microscopical Society 69:194–209.

14. 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.  Dissertation.  University of California, Santa Barbara, California, USA.

15. K. Whitney, unpublished data.

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

17. Dronen, N. O., and J. E. Badley.  1979.  Helminths of shorebirds from the Texas Gulf coast.  I.  Digenetic trematodes from the Long-billed curlew, Numenius americanus.  Journal of Parasitology 65:645–649.

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

19. J. Shaw and R. Hechinger, unpublished data.

20. Stunkard, H. W., and R. M. Cable.  1932.  The life history of Parorchis avitus (Linton), a trematode from the cloaca of the gull.  Biological Bulletin 62:328–338.

21. Cable, R. M., and W. E. Martin.  1935.  Parorchis avitus (Linton 1914), a synonym of P. acanthus (Nicoll, 1906).  Journal of Parasitology 21:436–437.

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

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

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

25. Armitage, M. H.  1999.  The euryhaline gobiid fish, Gillichthys mirabilis Cooper 1864, second intermediate host of the trematode, Pygidiopsoides spindalis Martin 1951.  Bulletin Southern California Academy of Sciences 98:75–79.

26. R. Hechinger and J. Shaw, unpublished data.

27. Martin W. E., and V. L. Gregory.  1951.  Cercaria buchanani n. sp., an aggregating marine trematode.  Transactions of the American Microscopical Society 70:359–362.

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



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