Microphallus piriformes
Encyclopedia
Microphallus piriformes is a parasitic trematode (fluke). It belongs to the Plagiorchiata
, a large suborder of the digenea
n fluke order
Plagiorchiida
. M. piriformes is unusual among the flukes in having only one intermediate host
rather than two, and no free-swimming cercarian stage.
It is most notable, however, for modifying the behaviour of its intermediate host in a way that increases its chance of transmission to the primary host. This has been researched by Helen O. McCarthy and her team of University of Ulster
scientists both in the laboratory
and at Muck Island
in Scotland
.
The life cycle
of M. piriformes requires two hosts: the Rough Periwinkle Littorina saxatilis (a littoral
snail
) and the Herring Gull Larus argentatus (and perhaps other members of the herring gull complex). The immature flukes live in the snail, and the adult flukes live in the bird
.
Normally, Rough Periwinkles are rarely eaten by Herring Gulls. This is due to two reasons: First, the birds forage in the snails' rocky shore habitat
mainly during the breeding season (which lasts about 4 months each summer) but not at other times. Second, periwinkle
s move with the tide
s to stay at the water line. Thus, even when the gulls forage in periwinkle habitat, the snails tend to stay out of easy reach of the birds.
It is not precisely known how the snails are infected; probably they eat the eggs directly from the gulls' feces
. The eggs hatch into a miracidium
stage, which develops into multiple sporocysts
. Rather than further developing into a cercaria which leaves the snail to infect the second intermediate host as usual for trematodes, they directly develop into encysted
metacercariae in the snail. Infection castrates the periwinkles; brood
ing L. saxatilis generally move only to avoid being left above water by the tide while non-brooding (including castrated) periwinkles are more active.
As soon as the flukes have reached the metacercarian stage, they alter the periwinkles' behaviour: Rather than moving to stay near the water line, the infected snails develop a pronounced tendency to move upwards. This becomes most pronounced shortly before high tide
, and thus the periwinkles carrying mature metacercariae are left a considerable distance above water when the tide recedes. This makes them far more accessible to the foraging gulls than uninfected conspecifics, which will often move up when the tide is highest to feed on algae which they cannot otherwise access, but return underwater as soon as the tide recedes to avoid desiccation
.
Once the snails are eaten by Herring Gulls, the metacercariae hatch into mature flukes. These mate and produce eggs which are shed with the bird's feces. Their adult lifespan is a mere two weeks; several generation
s are thus produced each summer. It is unknown whether M. piriformes spends the winter as resting eggs in the habitat, or as sporocysts in already-infected periwinkles. In any case, snails harboring metacercariae generally die of desiccation before winter if they are not eaten.
Plagiorchiata
The Plagiorchiata are by far the largest suborder of plagiorchiidan flatworms. They belong to the Digenea, a large subclass of flukes. These parasites rarely if ever affect humans, but domestic animals may be severely affected bby some species...
, a large suborder of the digenea
Digenea
Digenea is a subclass within the Platyhelminthes consisting of parasitic flatworms with a syncytial tegument and, usually, two suckers, one ventral and one oral. Adults are particularly common in the digestive tract, but occur throughout the organ systems of all classes of vertebrates...
n fluke order
Order (biology)
In scientific classification used in biology, the order is# a taxonomic rank used in the classification of organisms. Other well-known ranks are life, domain, kingdom, phylum, class, family, genus, and species, with order fitting in between class and family...
Plagiorchiida
Plagiorchiida
The Plagiorchiida are a large order of flatworms. They belong to the Digenea, a large subclass of flukes. Unlike the related Echinostomida and Strigeidida, they contain relatively few significant parasites of humans.The following suborders are placed here:...
. M. piriformes is unusual among the flukes in having only one intermediate host
Intermediate host
A secondary host or intermediate host is a host that harbors the parasite only for a short transition period, during which some developmental stage is completed. For trypanosomes, the cause of sleeping sickness, humans are the primary host, while the tsetse fly is the secondary host...
rather than two, and no free-swimming cercarian stage.
It is most notable, however, for modifying the behaviour of its intermediate host in a way that increases its chance of transmission to the primary host. This has been researched by Helen O. McCarthy and her team of University of Ulster
University of Ulster
The University of Ulster is a multi-campus, co-educational university located in Northern Ireland. It is the largest single university in Ireland, discounting the federal National University of Ireland...
scientists both in the laboratory
Laboratory
A laboratory is a facility that provides controlled conditions in which scientific research, experiments, and measurement may be performed. The title of laboratory is also used for certain other facilities where the processes or equipment used are similar to those in scientific laboratories...
and at Muck Island
Muck, Scotland
Muck is the smallest of four main islands in the Small Isles, part of the Inner Hebrides of Scotland. It measures roughly 2.5 miles east to west and has a population of around 30, mostly living near the harbour at Port Mòr. The other settlement on the island is the farm at Gallanach...
in Scotland
Scotland
Scotland is a country that is part of the United Kingdom. Occupying the northern third of the island of Great Britain, it shares a border with England to the south and is bounded by the North Sea to the east, the Atlantic Ocean to the north and west, and the North Channel and Irish Sea to the...
.
Ecology
Biological life cycle
A life cycle is a period involving all different generations of a species succeeding each other through means of reproduction, whether through asexual reproduction or sexual reproduction...
of M. piriformes requires two hosts: the Rough Periwinkle Littorina saxatilis (a littoral
Littoral
The littoral zone is that part of a sea, lake or river that is close to the shore. In coastal environments the littoral zone extends from the high water mark, which is rarely inundated, to shoreline areas that are permanently submerged. It always includes this intertidal zone and is often used to...
snail
Snail
Snail is a common name applied to most of the members of the molluscan class Gastropoda that have coiled shells in the adult stage. When the word is used in its most general sense, it includes sea snails, land snails and freshwater snails. The word snail without any qualifier is however more often...
) and the Herring Gull Larus argentatus (and perhaps other members of the herring gull complex). The immature flukes live in the snail, and the adult flukes live in the bird
Bird
Birds are feathered, winged, bipedal, endothermic , egg-laying, vertebrate animals. Around 10,000 living species and 188 families makes them the most speciose class of tetrapod vertebrates. They inhabit ecosystems across the globe, from the Arctic to the Antarctic. Extant birds range in size from...
.
Normally, Rough Periwinkles are rarely eaten by Herring Gulls. This is due to two reasons: First, the birds forage in the snails' rocky shore habitat
Habitat
* Habitat , a place where a species lives and grows*Human habitat, a place where humans live, work or play** Space habitat, a space station intended as a permanent settlement...
mainly during the breeding season (which lasts about 4 months each summer) but not at other times. Second, periwinkle
Common Periwinkle
The common periwinkle or winkle, scientific name Littorina littorea, is a species of small edible sea snail, a marine gastropod mollusk which has gills and an operculum, and is classified within the family Littorinidae, the periwinkles....
s move with the tide
Tide
Tides are the rise and fall of sea levels caused by the combined effects of the gravitational forces exerted by the moon and the sun and the rotation of the Earth....
s to stay at the water line. Thus, even when the gulls forage in periwinkle habitat, the snails tend to stay out of easy reach of the birds.
It is not precisely known how the snails are infected; probably they eat the eggs directly from the gulls' feces
Feces
Feces, faeces, or fæces is a waste product from an animal's digestive tract expelled through the anus or cloaca during defecation.-Etymology:...
. The eggs hatch into a miracidium
Miracidium
Trematodes are small parasitic flatworms that use vertebrates as their definitive host, and molluscs as their intermediate host. In order to accomplish this, they have several varied lifecyle stages....
stage, which develops into multiple sporocysts
Trematode lifecycle stages
Trematodes are small parasitic flatworms that use vertebrates as their definitive host, and molluscs as their intermediate host. In order to accomplish this, they have several varied lifecyle stages....
. Rather than further developing into a cercaria which leaves the snail to infect the second intermediate host as usual for trematodes, they directly develop into encysted
Cyst
A cyst is a closed sac, having a distinct membrane and division on the nearby tissue. It may contain air, fluids, or semi-solid material. A collection of pus is called an abscess, not a cyst. Once formed, a cyst could go away on its own or may have to be removed through surgery.- Locations :* Acne...
metacercariae in the snail. Infection castrates the periwinkles; brood
Avian incubation
Incubation refers to the process by which certain oviparous animals hatch their eggs, and to the development of the embryo within the egg. The most vital factor of incubation is the constant temperature required for its development over a specific period. Especially in domestic fowl, the act of...
ing L. saxatilis generally move only to avoid being left above water by the tide while non-brooding (including castrated) periwinkles are more active.
As soon as the flukes have reached the metacercarian stage, they alter the periwinkles' behaviour: Rather than moving to stay near the water line, the infected snails develop a pronounced tendency to move upwards. This becomes most pronounced shortly before high tide
High Tide
High Tide was a band formed in 1969 by Tony Hill , Simon House , Peter Pavli and Roger Hadden .-History:...
, and thus the periwinkles carrying mature metacercariae are left a considerable distance above water when the tide recedes. This makes them far more accessible to the foraging gulls than uninfected conspecifics, which will often move up when the tide is highest to feed on algae which they cannot otherwise access, but return underwater as soon as the tide recedes to avoid desiccation
Desiccation
Desiccation is the state of extreme dryness, or the process of extreme drying. A desiccant is a hygroscopic substance that induces or sustains such a state in its local vicinity in a moderately sealed container.-Science:...
.
Once the snails are eaten by Herring Gulls, the metacercariae hatch into mature flukes. These mate and produce eggs which are shed with the bird's feces. Their adult lifespan is a mere two weeks; several generation
Generation
Generation , also known as procreation in biological sciences, is the act of producing offspring....
s are thus produced each summer. It is unknown whether M. piriformes spends the winter as resting eggs in the habitat, or as sporocysts in already-infected periwinkles. In any case, snails harboring metacercariae generally die of desiccation before winter if they are not eaten.
See also
Other parasites that modify intermediate host behavior to facilitate transmission:- Dicrocoelium dendriticumDicrocoelium dendriticumThe Lancet liver fluke is a parasite fluke that tends to live in cattle or other grazing mammals.- History of discovery :...
, a fluke - Corynosoma constrictum, a thorny-headed worm
- Gynaecotyla aduncaGynaecotyla aduncaGynaecotyla adunca is a fluke that normally infects birds. It has also been found in 15% of a sample of the marsh rice rat from a salt marsh at Cedar Key, Florida. It uses fiddler crabs such as Uca rapax as its intermediate host.-Literature cited:*Kinsella, J.M. 1988...
, a fluke - Hymenolepis diminutaHymenolepis diminutaHymenolepis diminuta, also known as rat tapeworm, is a species of Hymenolepis tapeworm that causes hymenolepiasis. It has slightly bigger eggs and proglottids than H. nana and infects mammals using insects as intermediate hosts...
, a tapeworm - Polymorphus paradoxus, a thorny-headed worm