Leucochloridium variae

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Leucochloridium variae
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Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Platyhelminthes
Class: Trematoda
Order: Diplostomida
Family: Leucochloridiidae
Genus: Leucochloridium
Species:
L. variae
Binomial name
Leucochloridium variae
McIntosh, 1932 [1]

Leucochloridium variae, the brown-banded broodsac, is a species of trematode whose life cycle involves the alternate parasitic invasion of certain species of snail and bird. While there is no external evidence of the worm's existence within the bird host, the invasion of the snail host involves the grotesque swelling of one or both of the snail's eye stalks. This invasion does not cause the snail's death.

Contents

The swollen, pulsating eye stalk resembles a maggot or caterpillar. This modification attracts the parasite's definitive hosts, birds: the bird rips off the eye stalk and eats it, thus becoming infected with the sexually mature parasites. Later on the parasite's eggs are dropped with the bird's feces. Similar life-histories are found in other species in the genus Leucochloridium , including Leucochloridium paradoxum .

The snail regenerates a replacement eye stalk, which can also become reinfected by the parasite.

Taxonomy

Leucochloridium variae was described on the basis of adult flukes found in black-and-white warblers (Mniotilta varia) collected at Douglas Lake in northern Michigan, USA. [1] Two Nearctic species, Leucochloridium fuscostriatum Robinson, 1947 and Leucochloridium pricei McIntosh, 1932 are now considered to be synonyms of L. variae. [2] It has further been proposed that L. perturbatum Pojmańska, 1969, described from Europe, should be considered the same species even though gene flow between the populations will be limited by the few birds that cross between continents. [2] In the absence of genetic data, this synonymisation is still questioned. [3] Other European species already considered synonyms of L. perturbatum are L. subtilis Pojmańska, 1969 and L. fuscum Rietschel, 1970. [4] Leucochloridium sime Yamaguti, 1935 is also likely a synonym. [3]

Life-cycle

The lifecycle of L. variae is characterized by the infection of a definitive avian host through the ingestion of sporocysts contained in the intermediate Succinea host. Leucochloridium variae adults primarily live in the cloaca and intestine of their bird host, while the sporocysts live in the hepatopancreas, haemocoel and the ocular tentacles of Succineidae land snails. [5]

Transmission and infection of intermediate snail hosts

Avian hosts release fluke eggs along with their excreta, which land on surrounding vegetation where snails may consume them. The miracidia hatch and bore through the snail’s digestive tract. The sporocyst develop in the hepatopancreas of the snail. The sporocysts grow into a tree-like structure, with some branches growing through the haemocoel to form a swollen broodsac at the end of a long stalk. Cercariae are produced by asexual reproduction at the base of the sporocyst, then migrate into a brood sac; here they mature and encyst forming metacercariae. Brood-sacs insert into the snail’s tentacles, where they mimic the appearance and behavior of insect larvae so as to attract insectivorous birds. [6] [7] Snails can be infected by more than one species of Leucochloridium simultaneously. [8]

Broodsac description

Snails infected with the sporocyst exhibit distended tentacles, which disrupts the snail’s normal ability to retract into their shell. Broodsacs contain multiple free floating metacercariae. Light intensity affects the rate at which the broodsacs pulsate. Broodsacs normally pulsate between forty and eighty times per minute. The pulsating movement is described as an alternation of shortening and lengthening of the broodsac. Broodsacs do not pulsate in complete darkness. [9]

Transmission and infection of avian definitive hosts

The insectivorous birds are attracted to the pulsating broodsac. This will cause the birds to attack and ingest the broodsacs located in the snail's tentacles. Inside the bird's gut, the metacercariae develop into adults. Adult Leucochloridium variae are hermaphroditic helminths, but can cross fertilize with other worms if in close enough proximity. The gravid adults will release their eggs into the intestines of the bird to be excreted out with the bird’s feces; thus, continuing the Leucochloridium lifecycle. [10] Intense infection by the worms can lead emaciation and death in birds. Birds may also freeze to death from the lack of adipose tissue. [11]

Gravid adult description

Stages of the trematode life-cycle Trematode lifecycle stages.png
Stages of the trematode life-cycle

Adult worms are characterized by a flesh-colored body containing an egg-filled uterus that appears black by reflected light. The worms contain a cuticula with a subterminal oral sucker. They also contain a muscular pharynx, ventral sucker, and ceca. The gonads of the worm are arranged in a triangle, containing an ovary with an anterior and posterior testis. [9] The oral sucker is primarily used for the attachment to the avian cloaca. It must withstand the constriction of cloaca, which occurs during defecation. Leucochloridium contains a smooth oral sucker, which functions by forming a tight seal against the host’s mucosa. Leucochloridium also contains a smooth dorsal side, which aids in decreasing friction of passing stool. The rest of the fluke is covered in microvilli that are used to anchor it to the inside of the cloaca. Leucochloridium variae tegument is considered finely spined. [12]

Behavioral differences in infected intermediate hosts

Parasites may induce certain behavioral changes in their hosts in order to aid in the transmission and completion of its life cycle. Land snails parasitized by Leucochloridium spp. experience phenotypic modification through the pulsating brood sacs. Infected snails were found to have increased mobility, which allows them to migrate to higher and more well lit areas. Healthy snails seek darkness to hide from predators, but the infected amber snail moves itself into dangerous open and well lit spaces, thus making them more susceptible and accessible to avian predation. [13] [14]

Distribution and history

Leucochloridium variae commonly parasitizes Mniotilta varia and has been collected from lakes in the Michigan area. [7] [1] [15] Other known locations that L. variae are known to inhabit are Iowa, [16] Nebraska, [17] [2] Ohio [18] and others.

Hosts

Intermediate host of Leucochloridium variae include:

There was no finding of difference in length of shells in parasitized and in non-parasitized snails. [18]

Hosts of Leucochloridium variae include:

Related Research Articles

<span class="mw-page-title-main">Trematoda</span> Class of parasitic flatworms

Trematoda is a class of flatworms known as flukes or trematodes. They are obligate internal parasites with a complex life cycle requiring at least two hosts. The intermediate host, in which asexual reproduction occurs, is usually a snail. The definitive host, where the flukes sexually reproduce, is a vertebrate. Infection by trematodes can cause disease in all five traditional vertebrate classes: mammals, birds, amphibians, reptiles, and fish.

<span class="mw-page-title-main">Digenea</span> Class of flukes

Digenea is a class of trematodes in the Platyhelminthes phylum, consisting of parasitic flatworms with a syncytial tegument and, usually, two suckers, one ventral and one oral. Adults commonly live within the digestive tract, but occur throughout the organ systems of all classes of vertebrates. Once thought to be related to the Monogenea, it is now recognised that they are closest to the Aspidogastrea and that the Monogenea are more closely allied with the Cestoda. Around 6,000 species have been described to date.

<i>Fasciola hepatica</i> Species of fluke

Fasciola hepatica, also known as the common liver fluke or sheep liver fluke, is a parasitic trematode of the class Trematoda, phylum Platyhelminthes. It infects the livers of various mammals, including humans, and is transmitted by sheep and cattle to humans the world over. The disease caused by the fluke is called fasciolosis or fascioliasis, which is a type of helminthiasis and has been classified as a neglected tropical disease. Fasciolosis is currently classified as a plant/food-borne trematode infection, often acquired through eating the parasite's metacercariae encysted on plants. F. hepatica, which is distributed worldwide, has been known as an important parasite of sheep and cattle for decades and causes significant economic losses in these livestock species, up to £23 million in the UK alone. Because of its relatively large size and economic importance, it has been the subject of many scientific investigations and may be the best-known of any trematode species. F. hepatica's closest relative is Fasciola gigantica. These two flukes are sister species; they share many morphological features and can mate with each other.

<span class="mw-page-title-main">Aspidogastrea</span> Species of fluke

The Aspidogastrea is a small group of flukes comprising about 80 species. It is a subclass of the trematoda, and sister group to the Digenea. Species range in length from approximately one millimeter to several centimeters. They are parasites of freshwater and marine molluscs and vertebrates. Maturation may occur in the mollusc or vertebrate host. None of the species has any economic importance, but the group is of very great interest to biologists because it has several characters which appear to be archaic.

<span class="mw-page-title-main">Trematode life cycle stages</span>

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<i>Echinostoma</i> Genus of flukes

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<i>Leucochloridium</i> Genus of flukes

Leucochloridium is a genus of parasitic trematode worms in the order Diplostomida. It Is the sole genus in the family Leucochloridiidae. Members of this genus cause pulsating swellings in the eye-stalks of snails, so as to attract the attention of predatory birds required in the parasites' lifecycle.

<i>Brachylaima</i> Genus of flukes

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<i>Leucochloridium paradoxum</i> Parasitic flatworm

Leucochloridium paradoxum, the green-banded broodsac, is a parasitic flatworm. Its intermediate hosts are land snails, usually of the genus Succinea. The pulsating, green broodsacs fill the eye stalks of the snail, thereby attracting predation by birds, the primary host. These broodsacs visually imitate caterpillars, a prey of birds. The adult parasite lives in the bird's cloaca, releasing its eggs into the faeces.

Metagonimoides oregonensis is a trematode, or fluke worm, in the family Heterophyidae. This North American parasite is found primarily in the intestines of raccoons, American minks, frogs in the genus Rana, and freshwater snails in the genus Goniobasis. It was first described in 1931 by E. W. Price. The parasite has a large distribution, from Oregon to North Carolina. Adult flukes vary in host range and morphology dependent on the geographical location. This results in different life cycles, as well as intermediate hosts, across the United States. On the west coast, the intermediate host is freshwater snails (Goniobasis), while on the east coast the intermediate host is salamanders (Desmognathus). The parasites on the west coast are generally much larger than on the east coast. For example, the pharynx as well as the body of the parasite are distinctly larger in Oregon than in North Carolina. The reverse pattern is observed on the east coast for uterine eggs, which are larger on the west coast. In snails, there is also a higher rate of infection in female snails than in males. Research on the life history traits of the parasites have been performed with hamsters and frogs as model species.

<i>Novisuccinea ovalis</i> Species of gastropod

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<i>Bucephalus polymorphus</i> Species of fluke

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<i>Clinostomum marginatum</i> Species of fluke

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References

  1. 1 2 3 McIntosh, Allen (1932). "Some new species of trematode worms of the genus Leucochloridium Carus, parasitic in birds from Northern Michigan, with a key and notes on other species of the genus". Journal of Parasitology. 19 (1): 32–53. doi:10.2307/3271429. ISSN   0022-3395. JSTOR   3271429.
  2. 1 2 3 4 5 Bakke, T.A. (1982). "The morphology and taxonomy of Leucochloridium (L.) variae Mclntosh (Digenea, Leucochloridiidae) from the Nearctic as revealed by light and scanning electron microscopy". Zoologica Scripta. 11 (2): 87–100. doi:10.1111/j.1463-6409.1982.tb00521.x.
  3. 1 2 Nakao, M.; Sasaki, M.; Waki, T.; Iwaki, T.; Morii, Y.; Yanagida, K.; Watanabe, M.; Tsuchitani, Y.; Saito, T.; Asakawa, M. (2019). "Distribution records of three species of Leucochloridium (Trematoda: Leucochloridiidae) in Japan, with comments on their microtaxonomy and ecology". Parasitology International. 72: 101936. doi:10.1016/j.parint.2019.101936.
  4. ↑ Bakke, T.A. (1978). "Intraspecific variation of adult Leucochloridium sp. (Digenea) from natural and experimental infections". Canadian Journal of Zoology. 56 (1): 94–102. doi:10.1139/z78-013.
  5. ↑ Yamada, Seitaro; Fukumoto, Shin-ichiro (August 2011), "Isolation of sporocyst broodsacs of the genus Leucochloridium (Leucochloridiidae: Trematoda) from the intermediate host, Succunea lauta, in Japan", Japanese Journal of Veterinary Research, Graduate School of Veterinary Medicine, Hokkaido University, 59, doi:10.14943/jjvr.59.2-3.101
  6. ↑ Woodhead, Arthur E. (1935). "The mother sporocysts of Leucochloridium". The Journal of Parasitology. 21 (5): 337–346. doi:10.2307/3271943. ISSN   0022-3395. JSTOR   3271943.
  7. 1 2 McIntosh, Lois (1948). "Leucochloridium sporocysts from the Okoboji region". scholarworks.
  8. ↑ Ataev, G. L.; Zhukova, A. A.; Tokmakova, А. S.; Prokhorova, Е. E. (August 2016). "Multiple infection of amber Succinea putris snails with sporocysts of Leucochloridium spp. (Trematoda)". Parasitology Research. 115 (8): 3203–3208. doi:10.1007/s00436-016-5082-6. ISSN   0932-0113. PMID   27112757. S2CID   14985813.
  9. 1 2 Robinson, Edwin J. (1947). "Notes on the life history of Leucochloridium fuscostriatum n. sp. provis. (Trematoda: Brachylaemidae)". Journal of Parasitology. 33 (6): 467–475. doi:10.2307/3273326. ISSN   0022-3395. JSTOR   3273326. PMID   18903602.
  10. ↑ DeLaCruz, David. "Leucochloridium paradoxum". Animal Diversity Web. Retrieved 2020-02-27.
  11. ↑ Okulewicz, A.; Sitko, J. (2012-12-01). "Parasitic helminthes — probable cause of death of birds". Helminthologia. 49 (4): 241–246. doi: 10.2478/s11687-012-0045-7 . ISSN   1336-9083. S2CID   25123584.
  12. ↑ Bakke, T.A. (1976). "Functional morphology and surface topography of Leucochloridium sp. (Digenea), revealed by scanning electron microscopy". Zeitschrift für Parasitenkunde. 51 (1): 115–128. doi:10.1007/BF00380533. ISSN   0044-3255. S2CID   34328256.
  13. ↑ Wesołowska, W.; Wesołowski, T. (March 2014). "Do Leucochloridium sporocysts manipulate the behaviour of their snail hosts?: Leucochloridium sporocysts and snail host behaviour". Journal of Zoology. 292 (3): 151–155. doi: 10.1111/jzo.12094 .
  14. ↑ Staff, ZRS (2013-05-14). "ZOMBIE SNAILS SPREAD INFECTION".
  15. ↑ Lewis, Paul D. (1974). "Helminths of terrestrial molluscs in Nebraska. II. Life cycle of Leucochloridium variae McIntosh, 1932 (Digenea: Leucochloridiidae)". Journal of Parasitology. 60 (2): 251–255. doi:10.2307/3278459. ISSN   0022-3395. JSTOR   3278459. PMID   4821109.
  16. 1 2 Bernard Fried, Paul D. Lewis, Jr. and Kelly Beers 1995. Thin-Layer chromatographic and histochemical analyses of neutral lipids in the intramolluscan stages of Leucochloridium variae (Digenea, Leucochloridiidae) and the Snail Host, Succinea ovalis. Journal of Parasitology, volume 81(1): 112-114.
  17. ↑ Michael A. Barger & John A. Hnida. 2008. Survey of trematodes from terrestrial gastropods and small mammals in Southeastern Nebraska, U.S.A. Comparative Parasitology 75(2):308-314. doi:10.1654/4357.1
  18. 1 2 A Burky & Daniel J. Hornbach. 1979 Comparison of carbon and nitrogen content of infected and uninfected snails, Succinea ovalis, and the trematode Leucochloridium variae. Journal of Parasitology 65(3): 371-374
  19. ↑ Fried B., Beers K., Lewis PD Jr. 1993 (February). Lipids in the broodsac of Leucochloridium variae (Digenea, Leucochloridiidae) and its snail host Succinea ovalis. Int. J. Parasitol. 23(1):129-131.
  20. ↑ Parasites of the Robin Archived July 4, 2010, at the Wayback Machine . Accessed 12 February 2009.
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