Juga plicifera previously known as Oxytrema silicula is a fresh water aquatic snail. The common name for this species is the pleated juga. It is of interest to parasitologists in the US, as the first intermediate host of Nanophyetus salmincola, the fluke that harbors the rickettsiae responsible for salmon poisoning, elokomin fluke fever and the SF agent. By some accounts, the snail is also the first intermediate host of Acanthatrium oregonense, the fluke that harbors the rickettsia responsible for Potomac Horse fever. The genus Juga was formerly in the family Pleurocercidae. In the last decade, it was moved into the newly elevated Semisulcospiridae (formerly a subfamily within the Pleurocercidae).
Members of the family Semiculcospiridae are found in some Northern Hemisphere nations along the Pacific coast, i.e. the western United States, Vietnam, China, Japan and eastern Russia. The species Juga plicifera has a rather restricted distribution and is solely found in the north-western United States (in the states of Washington and Oregon). Being a freshwater snail, Juga plicifera prefers muddy sand bottoms of fresh water lakes and streams, but not shallow water. They feeds on dead vegetation and algae and are active throughout the year except winter.
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| Juga plicifera by Naturalis Biodiversity Center / CC0 via Wikimedia Commons |
Juga plicifera has a slender small to medium sized brown to black shell that is about an inch long (~35mm). It has ~15 whorls, which results in it being refer to as turriform. The whorls have raised ribs (called plicae, which are C-shaped) on them which are axial (parallel to the long axis of the shell). There are also finer cords on the outer most whorl perpendicular to the axis. It has an rounded aperture that forms an acute angle above. There is also an operculum that can be used to close the aperture.
My interest in the pleated Juga stems from its role in the life history of the trematode Nanophyetus salmincola. The trematode is a vector extraordinaire, which harbors more than one species of pathogenic rickettsia.
The life history of Nanophyetus salmincola was worked out by Bennington and Pratt in 1960. In a fantastic Journal of Parasitology article, they describe the life stages and development of the fluke. The trematode lays eggs that take >87 days to develop and hatch. Interestingly, the authors state that hatched miracidium were not attracted to the snails, but swam away after bumping into them. The authors found rediae and cercariae in all the tissues of infected snails. Only larger snails (>25 mm) shed ceracariae, and these were often shed with mucus, by the thousands, forming tiny ropes. It was noted that cercarial penetration of salmonid and non-salmonid fish such as goldfish and minnows resulted in fish death. N. salmincola could infect hamsters and wood rats but not mice in experimental infections. The encysted metacercariae are infective to dogs in which the trematode develops to adulthood, but the rickettsia Neorickettsia helminthoeca that lives obligately in the metacercaria of the fluke causes salmon poisoning.
Now, Nanophyetus salmincola also harbors another Neorickettsia that causes Elokomin fluke fever disease in bears, which is similar to salmon poisoning disease. More recently, Greiman et al. found that a third pathogenic Neorickettsia species was also vectored by the same fluke. This new rickettsia is called Stellanchasmus falcatus agent, and causes a mild fever in dogs. The SF agent was originally found in the fluke Stellanchasmus falcatus in Japan but has also been recorded in Metagonimoides oregonensis in Florida.
The literature on the exact association of Juga plicifera. and the trematode Acanthatrium oregonense is rather sparse. In a 1961 article (while J. plicifera was still called Oxytrema silicula), Burns notes that Acanthatrium oregonense cercariae were shed by O. silicula along with three other types of cercariae, which are not identified in the paper. In a 1998 paper, Barlough et al. identified N. risticii DNA by PCR in Juga hemphilli snails from Northern California. It seems possible that Acanthatrium uses many different species in the genus Juga as first intermediate hosts, and these associations may be worth studying.
In a captivating example of the complexity of parasitic life on the planet, the cercaria of Acanthatrium oregonense go on to penetrate caddisfly (genus Dicosmoecus) larvae, forming a motile metacercarie that eventually encysts in the thoracic muscles of the adult caddisflies. The metacercarie harbor Neorickettsia risticii, which causes Potomac horse fever when the caddisflies are accidentally ingested by horses. However, the trematode A. oregonense (of the family Lecithodendridae) is originally a parasite of bats and researchers have found that N. risticii is transmitted horizontally between bats, adding complexity to the epizootiology of Potomac horse fever. I believe it is entirely possible that other snails, arthropods and trematodes vector N. risticii, because Potomac horse fever is primarily a disease of the Eastern and South eastern US (Potomac, being a river of the eastern US), where Juga plicifera does not occur. In the meantime, I find the twice removed association of Juga and the various Neorickettsia to be wholly fascinating!
Refs:
Clarke, Arthur Haddleton. The freshwater molluscs of Canada. Canada Communication Group Pub, 1981.
Rudy Jr, Paul, et al. "Juga plicifera." Oregon Estuarine Invertebrates, Second Edition (2013).
Bennington, Elwin, and Ivan Pratt. "The life history of the salmon-poisoning fluke, Nanophyetus salmincola (Chapin)." The Journal of parasitology 46.1 (1960): 91-100.
Greiman, Stephen E., et al. "Nanophyetus salmincola, vector of the salmon poisoning disease agent Neorickettsia helminthoeca, harbors a second pathogenic Neorickettsia species." Veterinary parasitology 229 (2016): 107-109.
Barlough, Jeffrey E., et al. "Detection of Ehrlichia risticii, the agent of Potomac horse fever, in freshwater stream snails (Pleuroceridae: Juga spp.) from northern California." Appl. Environ. Microbiol. 64.8 (1998): 2888-2893.
Burns, William C. "Penetration and development of Allassogonoporus vespertilionis and Acanthatrium oregonense (Trematoda: Lecithodendriidae) cercariae in caddis fly larvae." The Journal of parasitology 47.6 (1961): 927-932.
Gibson, Kathryn E., et al. "Neorickettsia risticii is vertically transmitted in the trematode Acanthatrium oregonense and horizontally transmitted to bats." Environmental microbiology7.2 (2005): 203-212.
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