Weird Wacky Wonderful : Fascioloides magna - a giant of a fluke

One of the larger flukes familiar to veterinarians is the giant liver fluke of ungulates - Fascioloides magna, native to North America. It is also variously known as the deer fluke and large American liver fluke. The adult flukes may measure upto 10 cm, properly earning the species name magna. 

The major definitive host for this parasite is the white tailed deer (Odocoileus virginianus), but it can also infect black tailed deer (Odocoileus hemionus), wapitis (Cervus canadensis) and caribou (Rangifer tarandus) in North America. The fluke was introduced into Europe accidentally  in the 20th century and has been spreading, becoming common in some countries of eastern europe.  In Europe, hosts infected include the red deer (Capreolus elaphus), roe deer (Capreolus capreolus) and fallow deer (Dama dama).

Unlike the more popular and zoonotic Fasciola hepatica, adults of which live in the bile ducts, Fascioloides magna adults live in the parenchyma of the liver and are typically found in pseudo-fibrous cysts. These cysts are open/patent in deer but are not patent in domestic cattle, sheep to goats. Upto 4000 eggs may be shed through the patent openings in deer, pass into bile and from there into the feces. Due to the non-patent nature of infections in domestic ruminants, eggs cannot found in the feces in these hosts, unlike in deer.

Inside the eggs, a miracidium develops in the environment in 4-7 weeks, hatches by secreting proteolytic enzymes, swims in water to find a suitable snail intermediate host - of the genus Lymnaea. In the snail, the miracidium develops through the sporocyst (in the snail's pulmonary sac) and redia (in the snail's hepatopancreas) stages, eventually leaving the snail as a ceracaria in 6-9 weeks. The cercariae encyst onto grass, become meta-ceracariae and are eventually eaten by a susceptible host, ideally a deer. Inside the deer, the metacercaria migrate around, eventually entering the liver, where their movement provokes the formation of pseudocysts. Pseudocysts typically have more than one adult fluke. The prepatent period is variable, ranging between 3 and 7 months. 

The presence of the flukes do not affect deer to a large extent, which carry the small infections without clinical disease. Deer hunters may find the adult flukes in hunted deer. My PhD advisor shared a story of a hunter that he met in a small Wisconsin pub, who had just been imbibing after a deer hunt. The hunter appears to have been quite a foodie with an appetite for the extraordinary, evidenced by their description of how they absolutely loved the taste of the little butterflies in the liver of deer!

Just like with other parasites, the devil is in the numbers. Death can occur if there are hundreds of flukes. Egg production and the occurrence of the flukes as large foreign bodies in the liver are likely not good for the deer host. However, while severe clinical signs may not occur in North American wild ungulates (perhaps for lack of observation), clinical signs in european deer include typical non-specific signs such as reduced weight gain, poor ruts and poor antler quality. 

It is of interest to note that non-cervid ungulates get classified into aberrant and dead-end hosts for F. magna infections. Infection in aberrant hosts (domesticated sheep, goats and wild sheep) typically result in poor prognosis for these hosts due to liver damage, aberrant wanderings into other splanchnic organs, which may prove fatal. In dead-end large herbivore hosts such as cattle, bison, camelids, moose, pseudocysts form without an outlet, resulting in typical non-patent infections, unless the pseudocysts rupture. 

From a ecological stand point, it is to be noted that the fluke picks and chooses among several cervid options available on the continents as definitive hosts, and also picks specific species of snail hosts within the genus Lymnaea to use as first intermediate hosts, all in all contributing to its weirdness!

Ref:

Malcicka, Miriama. "Life history and biology of Fascioloides magna (Trematoda) and its native and exotic hosts." Ecology and evolution 5.7 (2015): 1381-1397.

Sound the ram's horn: Planorbella/Helisoma (Planorbidae)

The next snail species of interest once belonged to the genus Helisoma, but has recently been moved to the genus Planorbella. These are air-breathing freshwater snails. Two species in this genus are of interest as the first intermediate hosts of the carnivore trematode Alaria marcianae. These are Planorbella trivolvis and Planorbella campanulatum, commonly known as the marsh rams-horn and bell-mouth rams-horn respectively. However, the status of P. campanulatum as a valid species is under dispute.

Helisoma trivolvis
By Smithsonian Environmental
Research Center, CC BY 2.0
via Wikimedia Commons

Planorbella trivolvis looks a little different from the snails with spire-like shells that we have looked at before. Being a planorbid snail, it has a 15 - 18 mm flat coiling shell (called planispiral) with 3-4 whorls. And unlike the other snails, the shell is sinistral, i.e left-turning. It is light brown, dark brown, yellowish or chestnut colored. There are fine striae between the whorls. The mouth/aperture is large, with the lip being thickened internally, akin to a ram's horn/shofar. Both sexual and asexual reproduction is seen in these species and eggs are laid in small (~3mm) egg sacks.

Planorbella trivolvis is distributed throughout North America and has been introduced in other parts of the world. It prefers calm standing fresh waters (ecologically called "lentic") to running water (ecologically called "lotic"). The single foot allows locomotion under the surface of water.

In a 2007 survey of Planorbella snails from New Jersey, Klockars et al. recovered 8 types of cercariae. Two types of cercariae were identified as Echinostoma trivolis and Zygocotyle lunata while others were classified as armatae, brevifurcate apharyngeate, longifurcate pharyngate and brevifurcate pharyngate cercariae. Planorbella snails are first intermediate hosts of the following trematodes.

Helisoma trivolvis
By Say, 1817 -
Naturalis Biodiversity Center, CC0,
via Wikimedia Commons

1. Alaria:  As with other snails, Alaria miracidium infect the snail, develop thorough the sporocyst stage to become the cercarial stage, which are shed by the snail. The cercariae infect suitable amphibians such as tadpoles (frogs) and become the infective mesocercaria. Several other paratenic hosts can also be involved in this life cycle.

2. Zygocotyle lunata is a paramphistomid trematode found in the caecum of wild waterfowl (which are the definitive hosts) and may also incidentally affect ruminants. In North and South America, Z. lunata uses Planorbella as its first intermediate host. When Planorbella is not available, four species of Biomphalaria may serve as alternative first intermediate hosts. Z. lunata causes severe pathological changes in P. trivolvis and causes an apparent castration due to rupture and destruction of the snail's gonads.

3. Echinostoma trivolvis (and other related species) cause a zoonotic, intestinal food borne trematodiasis called echinostomiasis in humans and other vertebrate hosts. E. trivolvis uses amphibians and fish as second intermediate hosts. As with other food borne trematodiasis, humans become infected by consuming raw/undercooked second intermediate hosts. Symptoms point to a primarily gastrointestinal pathology in humans.

4. Bolbophorus confusus is a strigeoid trematode of American white pelicans (Pelicanus erythrorhynchous) that uses P. trivolvis as first intermediate host and about 28 species of fish as second intermediate hosts.

5. Riberoia ondatrae, a trematode that causes limb malformations in amphibians also uses P. trivolvis as intermediate host


References:
Fried, Bernard, et al. "The biology of the caecal trematode Zygocotyle lunata." Advances in Parasitology 69 (2009): 1-40.

Klockars, Jennifer, Jane Huffman, and Bernard Fried. "Survey of seasonal trematode infections in Helisoma trivolvis (Gastropoda) from lentic ecosystems in New Jersey, USA." Comparative Parasitology 74.1 (2007): 75-80.

Fox, Alfred Carter. The life cycle of Bolbophorus confusus (Krause, 1914) Dubois, 1935 (Tremotoda: Strigeoidea) and the effects of the metacercariae on fish hosts. Diss. Montana State University-Bozeman, College of Agriculture, 1965.

Johnson, Pieter TJ, et al. "Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States." Ecological Monographs 72.2 (2002): 151-168.

Yes, pleats. Let's talk about the fascinating pleated juga : Juga plicifera (Semisulcospiridae)

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. 

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.

Let's not gloss over the glossy pillars: Cochliocopa lubrica (Cochliocopidae)

Dicrocoelium dendriticum stages
and intermediate hosts
Acrylic on canvas by Jeba Jesudoss

Cochliocopa lubrica is also known as Cionella lubrica or the glossy pillar. It is a rather beautiful land snail species that is the intermediate host of the ruminant parasite – Dicrocoelium dendriticum and of the nematodes Protostrongylus rufescens, Meullerius capillaris, Elaphostrongylus cervi, Varestrongylus capreoli, Varestrongylus pneumonicus and Skrjabingylus nasicola. 

C. lubrica is a holarctic species found throughout North America, Europe, Africa, parts of Asia and New Zealand. In the United States, it is found on both sides of the continental divide. Being a land snail, it is found in forests and grassy areas, often close to human dwellings.

The snail is about 5 – 7 mm long and 2-3 mm wide. It has a brown ( ranging from off-white to almost amber), smooth, glossy, translucent shell which is bluntly rounded at the apex. There are 5-7 whorls. The opening/aperture is ovate and wide, and lacks denticles.  The soft parts of the body is dark blue-black.

Cochliocopa lubrica
Muséum national histoire naturelle /
CC BY
(https://creativecommons.org/licenses/by/4.0)
via Wikimedia

Experimental studies have shown that C. lubrica can tolerate high temperatures of 37 – 40 C and survive through a drought for 50 -70 days. However, snails infected with Dicrocoelium were less resistant than uninfected snails. 

While many other snail genera can be first intermediate hosts of D. dendriticium in parts of the world, C. lubrica is epizootically important in North America. For example, in a 1952 study on a heavily infected sheep farm in New York,  Mapes C.R. found that only C. lubrica out of 16 mollusc species studied harbored the sporocysts or cercariae of D. dendriticum. He also found that the distribution of the snail was similar to known areas where dicrocoeliasis occurred. 

Interestingly, C. lubrica is small enough to be preyed upon by other predator snails (a phenomenon called malacophagy). In experimental conditions, Nesovitrea hammonis (a snail found in Europe) was shown to be capable of preying upon C. lubrica, but not well enough to be a biological control agent. 

References:

Grewal, P. S., et al. "Parasitism of molluscs by nematodes: types of associations and evolutionary trends." Journal of Nematology 35.2 (2003): 146.

Badie, A., and Daniel Rondelaud. "Influence Du Parasitisme Sur La Résistance De Cionella Lubrica Müller A La Température Et A La Dessication." (1982).

Mapes, Cortland R. "Cionella lubrica (Muller), a new intermediate host of Dicrocoelium dendriticum (Rudolphi, 1819) Looss, 1899 (Treinatoda: Dicrocoeliidae)." Journal of Parasitology 38.1 (1952).

https://www.carnegiemnh.org/science/mollusks/va_cochlicopa_lubrica.html

http://fieldguide.mt.gov/speciesDetail.aspx?elcode=IMGAS11010

Snail Clone wars - Lymnaea cubensis and other look-alikes (Lymnaeidae)

Lymnaea cubensis
Antonio Alejandro Vázquez Perera
& Susana Perera Valderrama /
CC BY 3.0 via  Wikimedia Commons

The next snail in this series has many synonyms in literature. It has been called Galba cubensis, Bakerilymnaea cubensis, Fossaria cubensis and Lymnaea cubensis. I am going to refer to it as Lymnaea cubensis because the malacologists who have authored the book "Freshwater Gastropods of North America" call it that.  From the veterinary standpoint, L. cubensis is important as the first intermediate host of Heterobilharzia americana (along with another snail - Pseudosuccinea columella) and Fasciola hepatica.

The native range of L. cubensis is North and South America. In the United States, the snail is currently confined to the south and south east regions (The Carolinas, Georgia, Florida, Louisiana, Alabama, Texas, New Mexico and California). Due to anthropogenic introductions, L. cubensis was recorded in Spain by Schniebs et al. in 2018, which was the first time that it had been found in the wild in Europe.

L. truncatula
Francisco Welter Schultes, modified by Michal 
Maňas. Versión actual modified by Veronidae /
CC BY-SA 2.5 via Wikimedia Commons

L. schirazensis
María Dolores Bargues, Patricio Artigas,
Messaoud Khoubbane,  Rosmary Flores,
Peter Glöer, Raúl Rojas-García,
Keyhan Ashrafi, Gerhard Falkner,
Santiago Mas-Coma /
CC BY 2.5 via Wikimedia Commons

The snails are amphibious and are found in the mud in ditches and ponds. It is quite impossible to distinguish L. cubensis from L. truncatula based on shell morphology alone, and malacology training is required to identify the small differences in male reproductive system morphology between the two species as illustrated by Pointier et al. in their 2009 paper.

Interestingly, L. cubensis is not the only snail with striking morphological similarity to L. truncatula. A cryptic species with near worldwide distribution and very similar morphology called L. schirazensis was described in 2011 by Bargues et al. and is very resistant to Fasciola hepatica (i.e. no cercaria are produced). There are some serious complications that result from the identical morphologies of L. schirazensis and L. truncatula. Bargues et al. posit that misidentification of L. schirazensis as L. truncatula has distorted epidemiological data regarding snail susceptibility status to Fasciola. In the future, molecular data would have to be used to confirm  snail morphological identities in cases of cryptic species and the known occurrence of shape and size variations attributable to geography and lineage. PCR + sequencing of the coxI, ITS or 18S genes may help resolve identification problems, since it is well-known that the classification of the Lymnaeidae is fairly complicated (Link here for an explanation).

The capacity of L. cubensis in the transmission of the following is important:
(i)  Heterobilharzia americana: The role of L. cubensis was worked out in the early 1960s by Dr. Hong-Fong Lee. Furcocercous cercariae were shed 4 weeks after infection. Distribution of the trematode closely follows the distribution of its two first intermediate hosts: L. cubensis and P. columella.

(ii) Fascioloides magna: Vignoles et al. found that L. cubensis could be an experimental intermediate host for Fascioloides magna. The role played by the snail in natural infections is still unknown.

(iii) Fasciola hepatica: L. cubensis along with L. viatrix and L. neotropica have been established as the major vectors in Latin America. And while misidentifications of L. cubensis as L. truncatula may not throw-off the snail susceptibility data as much as L. schirazensis, the situation is still not ideal.

So, if you happen to be see a Lymnaeid snail that looks like L. truncatula, remember that identification to species level is very difficult and that the snail before you might not be the species that you think it is.

References:

Schniebs, Katrin, et al. "The first record of Galba cubensis (L. Pfeiffer, 1839)(Mollusca: Gastropoda: Lymnaeidae) from open fields of Europe." Folia Malacologica 26.1 (2018).

Dillon, Robert T. The freshwater gastropods of North America. Freshwater Gastropods of North America Project, 2019. FWGNA press. 

Lee, Hong-Fang. "Life history of Heterobilharzia americana Price 1929, a schistosome of the raccoon and other mammals in southeastern United States." The Journal of parasitology (1962): 728-739.

Vignoles, Philippe, et al. "Lymnaea cubensis, an experimental intermediate host for Fascioloides magna." Folia parasitologica 61.2 (2014): 185.

Bargues, M. D., et al. "Characterisation of Lymnaea cubensis, L. viatrix and L. neotropica n. sp., the main vectors of Fasciola hepatica in Latin America, by analysis of their ribosomal and mitochondrial DNA." Annals of Tropical Medicine & Parasitology 101.7 (2007): 621-641.

Don't pierce holes with this awl - Subulina octona (Subulinidae)

The next species of snail host extraordinaire first came to my attention as the first intermediate host of the feline trematode Platynosomum fastosum. It is known as the miniature awl snail or by its binomial name Subulina octona.

Subulina octona was originally native to the tropical parts of the Americas and the Caribbean. However, the current distribution is extensive due to introductions into other parts of the world. The snail has been reported in Europe (Denmark, Germany, Czech Republic), Sri Lanka and several island nations of Oceania such as Fiji, Samoa, Vanuatu etc. Whether the introductions were accidental or deliberate is currently unknown.

Subulina octona
By Luis Ruiz Berti, Creative Commons
CC BY-SA via Wikimedia

If you were to come across this terrestrial, air breathing snail you would observe the following. Subulina octona is an elegant, small snail measuring only 1.4 - 1.7 cms. The thin, glossy, pale yellow to brown shell is narrow, tapering and long with 8 - 11 whorls ending in an ovate aperture.

S. octona live in moist ground litter in forests but are also capable of thriving in greenhouses and hothouses. A distinctive feature of the life history that D'avila et al. record in their 2018 article involves "egg-retaining", which refers to a reproductive phenomenon in which a major part of the embryonic development occurs inside the body of the parent snail, and the egg when laid has a well-developed embryo. This strategy along with a long life span, several reproductive events per year and high survival of juveniles all result in S. octona being a successful invader.

This snail has an impressive ability to host parasites whose identities span both helminth phyla. It plays the role of intermediate host to trematodes, nematodes and cestodes including:

(1) Postharmostomum gallinarum, the cecal fluke of chickens, the life cycle of which involves S. octona and was worked out in Hawaii as early as 1940 by Dr. Joseph Alicata.

Subulina octona
By Bruguière, 1789 - Naturalis
Biodiversity Center,
Creative Commons CC0 via wikimedia

(2) Tamerlania bragai, the kidney fluke of domestic pigeons, the life cycle of which involves S. octona andwas worked out in Puerto Rico in 1945 by Dr. Jose Maldonado.

(3) Angiostrongylus cantonensis, the rat lungworm, which typically uses slugs and snails of other genera. A very interesting paper from Brazil by Caldeira et al. records S. octona as a naturally infected intermediate host of the A. cantonensis, harboring on average 20 L2/L3 larvae per snail.

(4) Angiostrongylus vasorum, the french heartworm: A paper published by Bessa et al. shows that S. octona infected with A. vasorum were capable of infecting a dog in an experimental setting, resulting in a patent infection in 49 days.

(5) Davainea proglottina: Cysticeroids of the poultry cestode Davainea were found in S. octona in Cuba. There was also a unique seasonal variation recorded by Perez et al, who observed cysticercoids only in February, May and August.

The wackiest thing about this snail is that there are sources (listed on the first page of a Google search) which sell awl snail adults for 2 Euros each (as of March 28, 2020). Buying and shipping this snail to your location is a terrible idea because it is a highly invasive species and considered an agricultural pest. There is certainly much ink spilled on the terrifying effects of introducing invasive species to novel non-native habitats, and the practice is not commendable.


References:
Title reference: The title of this post is a play on the common name of the snail (Miniature awl snail) and the small pointed tool used for piercing holes called the awl.

Juřičková, L. U. C. I. E. "Subulina octona (Bruguière, 1798)–a new greenhouse species for the Czech Republic (Mollusca: Gastropoda: Subulinidae)." Malacologica Bohemoslovaca 5 (2006): 1-2.

D’ávila, Sthefane, et al. "Life history of Subulina octona (Brugüière)(Gastropoda: Pulmonata: Subulinidae) based on four-year laboratory observations and a comparative histological analysis of egg-retaining and ovoviviparous subulinids." Journal of Natural History 52.23-24 (2018): 1551-1569.

Alicata, Joseph E. "The life cycle of Postharmostomum gallinum, the cecal fluke of poultry." The Journal of Parasitology 26.2 (1940): 135-143.
Maldonado, José F. "The life cycle of Tamerlania bragai, Santos 1934,(Eucotylidae), a kidney fluke of domestic pigeons." The Journal of Parasitology 31.5 (1945): 306-314.

Caldeira, Roberta Lima, et al. "First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935)(Nematoda: Metastrongylidae) in Brazil." Memórias do Instituto Oswaldo Cruz 102.7 (2007): 887-889.

Bessa, EC de A., et al. "Biological development of Angiostrongylus vasorum (Baillet) Kamensky (Nematoda, Metastrongylidae) in Subulina octona Bruguière (Mollusca, Subulinidae) in laboratory conditions." Revista Brasileira de Zoologia 17.1 (2000): 29-41.

Perez, A., et al. "Seasonal dynamics of the cysticercoids of Davainea proglottina in the intermediate host Subulina octona." Revista Avicultura, Cuba 24.3/4 (1980): 223-225.

Slender walkers are moonwalkers: Pomatiopsis lapidaria (Pomatiopsidae)

Continuing our intellectually profitable exercise of studying snail intermediate hosts brings us to our next snail - Pomatiopsis lapidaria, also known as the slender walker. This freshwater amphibious snail is the first intermediate host of the lung trematode of the mammals of North America - Paragonimus kellicotti.

Pomatiopsis lapidaria
by John Slapcinsky under CreativeCommons 
CC BY-NC-SA 3.0
via boldsystems.org

Members of the genus Pomatiopsis are restricted to the temperate portions of North America and there are atleast five species : P. lapidaria, P. californica, P. cincinnatiensis, P. chacei and P. binneyi. The distribution of P. lapidaria is skewed and populations occur mostly in the eastern United States with the western borders of the distribution being in Iowa, Missouri, Kansas, Texas and New Mexico.  

 Pomatiopsis lapidaria
by Smithsonian Institution NMNH, 
under CreativeCommons
CC BY-NC-SA 3.0 via eol.org

P. lapidaria are small, thin, operculate (having a small lid that closes the aperture of the shell) dark brown-colored snails, on average about a fifth of an inch in length but never more than 8 mm. According to the original species description published by Say in 1817, the shell is turreted with a raised spire with six revolutions/whorls. The coiling is right handed (dextral). The shell surface has wrinkles/growth-lines across it and the sutures are impressed. The opening or aperture is ovate with a lip that is simple or slightly reflected. Gills may be seen in live specimens. These snails are different from the Lymnaidae in that they are sexually dimorphic. Males are more slender and may have more whorls than females.

It is interesting to note that P. lapidaria are said to have a characteristic "loping" movement, which involves large arching waves of motion that results in unusually rapid progression. This seems to be a characteristic of other land snails as well. Additionally, these are amphibious snails, and controversies have raged in the past about their terrestrial/aquatic habitat preferences. The species also seems to be nocturnal in its habits, hiding under leaves on bright days and being active on warm humid evenings in areas with moist marshy soils. They are also able to withstand long periods of dessication and are capable of being laboratory reared for experimental purposes.

As a veterinary parasitologist, I find it incredibly important to understand the vectorial capacity of this snail. These are several mentions of experiments from the world war II era in which attempts were made to determine if P. lapidaria was a vector of Schistosoma japonicum (the "Oriental" blood fluke). The basis for these experiments stemmed from the ecological and morphological similarity of P. lapidaria to Oncomelania, another member of the Pomatiopsidae, found in east Asia, which is known to be a competent vector of S. japonicum. However, it was found that only 5 out of 2000 experimentally infected P. lapidaria could shed S. japonicum cercaria, making the snail a poorly adapted vector.  However, the snail is intermediate host extraordinaire for Paragonimus kellicotti, Nudocotyle novicia (a bile duct fluke of meadow mice) and Euhryhelmis monorchis (a mink trematode).

From a public health perspective, it is important to note that Paragonimus kellicotti is an endemic trematodiasis that can affect humans in North America who consume raw or undercooked crayfish containing the infective metacercaria of the fluke. While the trematode can complete its life-cycle in humans resulting in patent infections, ectopic migration can cause trematode larval migrans (when the flukes migrate in subcutaneous tissues) and cerebral paragonimiasis, which are both rare in dogs, cats and other animals. The second intermediate hosts are crustaceans (crayfish) of the genera Oronectes and Cambarus, in which the metacercaria have a predilection for the crustacean heart. Humans infections have been reviewed in a fantastic paper by Diaz J. in the journal Clinical microbiology reviews (Link here). 

References:

Title reference: The title of this post is a play on the common name of the snail (Slender walkers) and their ability to move by loping, which is a motion almost as unique as the dance move called "moon-walk" of wide pop-cultural fame. The snails are also nocturnal, which helps with the moon walking theme.

Say, Thomas. Description of Seven Species of American Frech-water and Land Shells, Not Noticed in the Systems. 1817.

Dundee, Dee Saunders. "Aspects of the biology of Pomatiopsis lapidaria (Say)(Mollusca: Gastropoda: Prosobranchia)." (1957).

Parker, George Howard. "The loping of land-snails." The Biological Bulletin 72.3 (1937): 287-289.

Ameel, Donald J. "Observations on the natural history of Pomatiopsis lapidaria Say." American Midland Naturalist 19.3 (1938): 702-705.

DeWitt, William B. "Pomatiopsis lapidaria, its occurrence in the Washington, DC area and its laboratory rearing in comparison to that of Oncomelania spp." The Journal of parasitology 38.4 (1952): 321-326.

Walker, Bryant, Charles Keene Dodge, and Edward Bruce Williamson. A Synopsis of the Classification of the Fresh-water Mollusca of North America, North of Mexico: And A Catalogue of the More Recently Described Species, with Notes. No. 1-6. The University, 1916.

Diaz, James H. "Paragonimiasis acquired in the United States: native and nonnative species." Clinical microbiology reviews 26.3 (2013): 493-504.
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