Ribeiroia Marini
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''Ribeiroia'' () is a genus of trematode
parasite Parasitism is a Symbiosis, close relationship between species, where one organism, the parasite, lives (at least some of the time) on or inside another organism, the Host (biology), host, causing it some harm, and is Adaptation, adapted str ...
s that sequentially infect
freshwater snail Freshwater snails are gastropod mollusks that live in fresh water. There are many different families. They are found throughout the world in various habitats, ranging from ephemeral pools to the largest lakes, and from small seeps and springs t ...
s in the family
Planorbidae Planorbidae, common name the ramshorn snails or ram's horn snails, is a family (biology), family of air-breathing freshwater snails, Aquatic animal, aquatic pulmonate gastropod Mollusca, molluscs. Unlike most molluscs, the blood of ram's horn sn ...
(ramshorn snails) as first intermediate
hosts A host is a person responsible for guests at an event or for providing hospitality during it. Host may also refer to: Places * Host, Pennsylvania, a village in Berks County * Host Island, in the Wilhelm Archipelago, Antarctica People * ...
,
fish A fish (: fish or fishes) is an aquatic animal, aquatic, Anamniotes, anamniotic, gill-bearing vertebrate animal with swimming fish fin, fins and craniate, a hard skull, but lacking limb (anatomy), limbs with digit (anatomy), digits. Fish can ...
and larval
amphibian Amphibians are ectothermic, anamniote, anamniotic, tetrapod, four-limbed vertebrate animals that constitute the class (biology), class Amphibia. In its broadest sense, it is a paraphyletic group encompassing all Tetrapod, tetrapods, but excl ...
s as second intermediate hosts, and
birds Birds are a group of warm-blooded vertebrates constituting the class (biology), class Aves (), characterised by feathers, toothless beaked jaws, the Oviparity, laying of Eggshell, hard-shelled eggs, a high Metabolism, metabolic rate, a fou ...
and
mammals A mammal () is a vertebrate animal of the class Mammalia (). Mammals are characterised by the presence of milk-producing mammary glands for feeding their young, a broad neocortex region of the brain, fur or hair, and three middle e ...
as definitive hosts (see ). In
North America North America is a continent in the Northern Hemisphere, Northern and Western Hemisphere, Western hemispheres. North America is bordered to the north by the Arctic Ocean, to the east by the Atlantic Ocean, to the southeast by South Ameri ...
, infection by ''Ribeiroia'' has been linked to amphibians with limb
malformations A birth defect is an abnormal condition that is present at birth, regardless of its cause. Birth defects may result in disabilities Disability is the experience of any condition that makes it more difficult for a person to do certain act ...
. The connection between
parasitic infection A parasitic disease, also known as parasitosis, is an infectious disease caused by parasites. Parasites are organisms which derive sustenance from its host while causing it harm. The study of parasites and parasitic diseases is known as parasitolog ...
and limb malformations has generated questions about (a) whether parasite-induced malformations in amphibians are increasing (see ), and (b) the consequences of such abnormalities for amphibian population conservation (see ).


Taxonomy

''Ribeiroia'' is a genus of parasites in the class
Trematoda Trematoda is a class of flatworms known as trematodes, and commonly as flukes. They are obligate internal parasites with a complex life cycle requiring at least two hosts. The intermediate host, in which asexual reproduction occurs, is a mol ...
, phylum
Platyhelminthes Platyhelminthes (from the Greek πλατύ, ''platy'', meaning "flat" and ἕλμινς (root: ἑλμινθ-), ''helminth-'', meaning "worm") is a phylum of relatively simple bilaterian, unsegmented, soft-bodied invertebrates commonly called f ...
. Currently three species and one
subspecies In Taxonomy (biology), biological classification, subspecies (: subspecies) is a rank below species, used for populations that live in different areas and vary in size, shape, or other physical characteristics (Morphology (biology), morpholog ...
of ''Ribeiroia'' are recognized: '' R. ondatrae'' in North America, ''R. marini'' in the Caribbean, ''R. m. guadeloupensis'' on the Caribbean island of
Guadeloupe Guadeloupe is an Overseas departments and regions of France, overseas department and region of France in the Caribbean. It consists of six inhabited islands—Basse-Terre Island, Basse-Terre, Grande-Terre, Guadeloupe, Grande-Terre, Marie-Galant ...
, and ''R. congolensis'' in Africa (Johnson et al. 2004). The trematode ''Cercaria lileta'' is also closely related to ''Ribeiroia'', and molecular sequence data indicates that it may be a species of ''Ribeiroia'' (Johnson et al. 2004). All species of ''Ribeiroia'' share the distinctive morphological characteristic of esophageal diverticula (i.e., two short dead-end branches that extend laterally from the
esophagus The esophagus (American English), oesophagus (British English), or œsophagus (Œ, archaic spelling) (American and British English spelling differences#ae and oe, see spelling difference) all ; : ((o)e)(œ)sophagi or ((o)e)(œ)sophaguses), c ...
). Other genera closely related to ''Ribeiroia'' include '' Cladocystis trifolium'', '' Cathemasia'', and ''
Echinostoma ''Echinostoma'' is a genus of Trematoda, trematodes (flukes), which can infect both humans and other animals. These intestinal trematoda, flukes have a three-host life cycle with snails or other aquatic organisms as intermediate hosts, and a var ...
'' (Johnson et al. 2004). See Johnson et al. (2004) for more details on morphological and ecological differences as well as
phylogenetic In biology, phylogenetics () is the study of the evolutionary history of life using observable characteristics of organisms (or genes), which is known as phylogenetic inference. It infers the relationship among organisms based on empirical dat ...
relationships between these species.


Life cycle

''Ribeiroia ondatrae'' has an indirect complex life cycle. The adult worms live inside predatory birds or mammals (the definitive hosts), wherein they reproduce sexually if other worms are present. Mature adults release eggs into the host’s intestinal tract, which are passed with the feces of the host, and to develop need to end up in water. The eggs typically develop in 2–3 weeks, but the time varies depending on water temperature. Eggs hatch into
miracidia The miracidium is the second stage in the life cycle of trematodes. When trematode eggs are laid and come into contact with fresh water, they hatch and release miracidium. In this phase, miracidia are ciliated and free-swimming. This stage is comp ...
, a ciliated free-living parasite stage, which infect the first intermediate host, ram’s horn snails in the family
Planorbidae Planorbidae, common name the ramshorn snails or ram's horn snails, is a family (biology), family of air-breathing freshwater snails, Aquatic animal, aquatic pulmonate gastropod Mollusca, molluscs. Unlike most molluscs, the blood of ram's horn sn ...
, colonizing the snail’s reproductive tissue and eventually forming rediae, a slow-moving worm-like parasite stage. The rediae reproduce asexually, castrating the snail as they feed on its reproductive tissue. The infection becomes mature in about six weeks, when the rediae within the snail begin to release a second free-swimming stage called
cercaria A cercaria (plural cercariae) is a larval form of the trematode class of parasites. It develops within the germinal cells of the Trematode life cycle stages, sporocyst or redia. A cercaria has a tapering head with large penetration glands. It may ...
e. The key identifying characteristic of ''Ribeiroia ondatrae'' cercariae is the bifurcated esophagus (although this trait can occur in some closely related genera such as '' Cladocystis trifolium''). Cercariae infect amphibians or fish (the second intermediate hosts) wherein they encyst in (with amphibians) the
limb bud The limb bud is a structure formed early in vertebrate limb development. As a result of interactions between the ectoderm and underlying mesoderm, formation occurs roughly around the fourth week of development. In human embryonic development, the ...
s or (with fish) along the
lateral line The lateral line, also called the lateral line organ (LLO), is a system of sensory organs found in fish, used to detect movement, vibration, and pressure gradients in the surrounding water. The sensory ability is achieved via modified epithelia ...
and scales of the head, body and gills. Encysted cercariae become metacercariae, a dormant
parasite Parasitism is a Symbiosis, close relationship between species, where one organism, the parasite, lives (at least some of the time) on or inside another organism, the Host (biology), host, causing it some harm, and is Adaptation, adapted str ...
stage with a thin outer
membrane A membrane is a selective barrier; it allows some things to pass through but stops others. Such things may be molecules, ions, or other small particles. Membranes can be generally classified into synthetic membranes and biological membranes. Bi ...
. Metacercariae resemble cercariae without their tails and do not reproduce. The definitive hosts (birds and mammals) become infected when they consume an amphibian or fish that has encysted metacercariae. The life cycle is completed when the metacercariae emerge from their cyst and attach to the definitive host’s intestinal tract and develop into adults, typically in the
proventriculus The proventriculus is part of the digestive system of birds.Encarta World English Dictionary orth American Edition(2007). ''Proventriculus''. Source: (accessed: December 18, 2007) An analogous organ exists in invertebrates and insects. Birds Th ...
of birds and the stomach of mammals.


Infection and amphibian malformations


Laboratory studies

Experimental exposure to ''Ribeiroia ondatrae'' cercariae has been shown to cause limb malformations in various frog, toad and
salamander Salamanders are a group of amphibians typically characterized by their lizard-like appearance, with slender bodies, blunt snouts, short limbs projecting at right angles to the body, and the presence of a tail in both larvae and adults. All t ...
species, including '' Pseudacris regilla, Anaxyrus boreas,
Lithobates ''Lithobates'', commonly known as the bullfrogs, is a genus of true frogs, of the family Ranidae. The name is derived from '' litho-'' (stone) and the Greek ' (, one that treads), meaning one that treads on rock, or rock climber. As presently de ...
pipiens, A. americanus, Ambystoma macrodactylum, L. clamitans'' and ''L. sylvatica''. Cercariae appear to prefer to infect in and around the developing limb buds of larval amphibians, which can alter or inhibit limb development. The risk of malformation and mortality varies as a function of parasite exposure level, host development stage, and the amphibian species involved. As expected for macroparasitic infections, a dose-dependent relationship exists between cercariae exposure and pathology, particularly among larval amphibians at pre- or early-limb development stage. Cercarial penetration of host tissue involves
proteolytic Proteolysis is the breakdown of proteins into smaller polypeptides or amino acids. Protein degradation is a major regulatory mechanism of gene expression and contributes substantially to shaping mammalian proteomes. Uncatalysed, the hydrolysis o ...
enzymes. The exact mechanism which alters limb development is unknown, but potential pathways include mechanical disturbance by invading parasites, release of a teratogenic chemical by parasites, or a combination of the two. Susceptibility to infection and the subsequent pathology differs among amphibian species. For example, gray tree frogs (''
Hyla versicolor ''Hyla'' is a genus of frogs in the tree frog family Hylidae. As traditionally defined, it was a wastebasket genus with more than 300 species found in Europe, Asia, Africa, and across the Americas. After a major revision of the family, most of t ...
'') are largely resistant to infection, but toads (e.g. ''A. americanus'') exhibit high frequencies of mortality and malformations following parasite exposure (Johnson and Hartson 2009). The types of limb malformations also vary among species and developmental stage of exposure. The most common errors in development associated with ''Ribeiroia'' exposure are skin webbings (cutaneous fusion), missing limbs and limb elements ( ectromelia and
hemimelia Hemimelia is a birth defect consisting in unilateral or bilateral underdevelopment of the distal part of the lower or upper limb. The affected bone may be shortened or not develop at all. Types of hemimelia Transverse hemimelia is a congenital ...
), supernumerary limbs and digits (
polymelia Polymelia is a birth defect in which an affected individual has more than the usual number of limbs. It is a type of dysmelia. In humans and most land-dwelling vertebrates, this means having five or more limbs. The extra limb is most commonly shr ...
and
polydactyly Polydactyly is a birth defect that results in extra fingers or toes. The hands are more commonly involved than the feet. Extra fingers may be painful, affect self-esteem, or result in clumsiness. It is associated with at least 39 genetic mut ...
), and bony triangles. The factors determining variation in susceptibility among species remain poorly understood. However these observations suggest that the type of malformation alone is unlikely to be diagnostic of ''Ribeiroia'' exposure.


Field studies

''Ribeiroia'' infection has been linked to malformations in naturally occurring amphibian populations, especially in the
western Western may refer to: Places *Western, Nebraska, a village in the US *Western, New York, a town in the US *Western Creek, Tasmania, a locality in Australia *Western Junction, Tasmania, a locality in Australia *Western world, countries that id ...
and
midwestern The Midwestern United States (also referred to as the Midwest, the Heartland or the American Midwest) is one of the four census regions defined by the United States Census Bureau. It occupies the northern central part of the United States. It ...
US. In a large-scale study in the western US, both the presence and abundance of ''Ribeiroia'' infection predicted higher-than-baseline (e.g. >5%) frequencies of abnormalities in one or more amphibian species. Limb malformations were observed in nine species and ranged in frequency from <5% to nearly 90%. The role of ''Ribeiroia'' in explaining accounts of amphibian malformations in other regions is varied; ''Ribeiroia'' has been associated with malformation "hotspots" in the midwestern and northeastern US, but it was not detected in malformation surveys from
Vermont Vermont () is a U.S. state, state in the New England region of the Northeastern United States. It borders Massachusetts to the south, New Hampshire to the east, New York (state), New York to the west, and the Provinces and territories of Ca ...
,
Alaska Alaska ( ) is a non-contiguous U.S. state on the northwest extremity of North America. Part of the Western United States region, it is one of the two non-contiguous U.S. states, alongside Hawaii. Alaska is also considered to be the north ...
,
Bermuda Bermuda is a British Overseas Territories, British Overseas Territory in the Atlantic Ocean, North Atlantic Ocean. The closest land outside the territory is in the American state of North Carolina, about to the west-northwest. Bermuda is an ...
, and
Michigan Michigan ( ) is a peninsular U.S. state, state in the Great Lakes region, Great Lakes region of the Upper Midwest, Upper Midwestern United States. It shares water and land boundaries with Minnesota to the northwest, Wisconsin to the west, ...
.Gilliland and Muzzall 2002; Bacon et al. 2006; Skelly et al. 2007; Reeves et al. 2008


Geographic distribution

''Ribeiroia ondatrae'' is widely distributed across the US, including records from 22 species in 37 states (Johnson and McKenzie 2008). Most records of ''Ribeiroia''-associated malformations have been reported from California, Oregon, Washington, Montana, Minnesota, Wisconsin, New Jersey and Pennsylvania. Less is known about the distribution of ''Ribeiroia'' in Canada and Central America. In amphibians, both the abundance of the parasite and the number of observations appear to correlate positively with major bird migratory
flyway A flyway is a flight path used by large numbers of birds while migrating between their breeding grounds and their overwintering quarters. Flyways generally span continents and often pass over oceans. Although applying to any species of migrat ...
s, with concentrations along the
Pacific The Pacific Ocean is the largest and deepest of Earth's five oceanic divisions. It extends from the Arctic Ocean in the north to the Southern Ocean, or, depending on the definition, to Antarctica in the south, and is bounded by the cont ...
,
Mississippi Mississippi ( ) is a U.S. state, state in the Southeastern United States, Southeastern and Deep South regions of the United States. It borders Tennessee to the north, Alabama to the east, the Gulf of Mexico to the south, Louisiana to the s ...
, and
Atlantic The Atlantic Ocean is the second largest of the world's five oceanic divisions, with an area of about . It covers approximately 17% of Earth's surface and about 24% of its water surface area. During the Age of Discovery, it was known for se ...
flyways (Johnson et al. 2010). This observation suggests definitive (bird) host activity is an important determinant of parasite distribution at the continental scale, but this hypothesis has yet to be rigorously tested. ''Ribeiroia ondatrae'' is most often recovered from amphibians in lentic habitats, such as ponds, lakes, and wetlands, which support planorbid snails. Other species of Ribeiroia occur in the Caribbean and South America (''R. marini'' and ''R. marini guadeloupensis'') and in Africa (''R. congolensis''). However, whether these species infect amphibians or cause limb malformations has not been explored.


Evidence for emergence

Dating back over 200 years, there have been reports of amphibian malformations suggesting that the general phenomenon is not a new occurrence in amphibian populations (Ouellet 2000). Despite the historical occurrence of amphibian malformations, the real question is whether such malformations are increasing in
prevalence In epidemiology, prevalence is the proportion of a particular population found to be affected by a medical condition (typically a disease or a risk factor such as smoking or seatbelt use) at a specific time. It is derived by comparing the number o ...
and severity in wild amphibian populations. Limited historical data on malformations and the absence of baseline malformation data has complicated attempts to assess whether malformations are emerging. However, research over the past decade has shown that malformations are emerging in some amphibian populations. For example, the background rate of malformations of northern leopard frogs in
Minnesota Minnesota ( ) is a U.S. state, state in the Upper Midwestern region of the United States. It is bordered by the Canadian provinces of Manitoba and Ontario to the north and east and by the U.S. states of Wisconsin to the east, Iowa to the so ...
increased from 0.4% in 1958–1963 to 2.5% in 1996–1997 (Hoppe 2000), with recently observed malformations more severe and more diverse. Similarly, Johnson and Lunde (2005), in a comparison of recent (1990–2000) and historical (1899–1989) publications, found that recent reports document: # a wider range of more severe malformations, # a greater number of affected amphibian species, # a larger number of affected sites, and # a higher frequency range of affected individuals at reported sites. For both of these studies, however, the mechanisms driving the apparent increase in malformations were not identified (see Factors influencing emergence). In a more rigorous study, Johnson et al. (2003) confirmed that historical malformations at six of eight sites (1947–1990) were associated with ''Ribeiroia'' infection. Moreover, three of these sites continued to support limb malformations at frequencies of 7-50% in one or more species. One pond in particular (Jette Pond in western Montana) showed increased prevalence of malformations in '' Pseudacris regila'' from 20% in 1960 to 46% in 2000, which was correlated with an increased intensity of ''Ribeiroia'' infection. Although more research is necessary, these studies provide evidence that malformations, especially those linked to ''Ribeiroia'' infection, are emerging in some amphibian populations.


Factors influencing infection

Nutrients -
Nitrogen Nitrogen is a chemical element; it has Symbol (chemistry), symbol N and atomic number 7. Nitrogen is a Nonmetal (chemistry), nonmetal and the lightest member of pnictogen, group 15 of the periodic table, often called the Pnictogen, pnictogens. ...
and
phosphorus Phosphorus is a chemical element; it has Chemical symbol, symbol P and atomic number 15. All elemental forms of phosphorus are highly Reactivity (chemistry), reactive and are therefore never found in nature. They can nevertheless be prepared ar ...
enrichment are widespread forms of anthropogenic environmental change that may influence parasite infection (Johnson and Carpenter 2008). Nutrient enrichment leads to
eutrophication Eutrophication is a general term describing a process in which nutrients accumulate in a body of water, resulting in an increased growth of organisms that may deplete the oxygen in the water; ie. the process of too many plants growing on the s ...
, which has been linked with emergence of ''Ribeiroia ondatrae'' through direct and indirect effects on aquatic
food web A food web is the natural interconnection of food chains and a graphical representation of what-eats-what in an ecological community. Position in the food web, or trophic level, is used in ecology to broadly classify organisms as autotrophs or he ...
s (Johnson and Chase 2004). The underlying mechanism through which eutrophication can increase infection involves increasing the density of infected first-intermediate snail hosts and by increasing the production of parasites by infected snails (Johnson et al. 2007). Pesticides -
Pesticide Pesticides are substances that are used to control pests. They include herbicides, insecticides, nematicides, fungicides, and many others (see table). The most common of these are herbicides, which account for approximately 50% of all p ...
s are still considered a potential factor influencing amphibian malformations (Johnson et al. 2010). However, recent investigations have focused on the interaction of pesticides with parasite infection (Kiesecker 2002; Rohr et al. 2008). Field experiments indicated a link between agricultural run-off and increased infection (Kiesecker 2002). Laboratory studies further demonstrated that pesticide exposure reduced host
immunocompetence In immunology, immunocompetence is the ability of the body to produce a normal immune response following exposure to an antigen. Immunocompetence is the opposite of immunodeficiency (also known as ''immuno-incompetence'' or being ''immuno-compro ...
against parasites as the biological mechanism (Kiesecker 2002). Furthermore, there may be a link between nutrient addition and pesticide contamination jointly leading to increased infections by simultaneously increasing exposure and suppressing host immune systems (Rohr et al. 2008a, b). Biodiversity - Host species
diversity Diversity, diversify, or diverse may refer to: Business *Diversity (business), the inclusion of people of different identities (ethnicity, gender, age) in the workforce *Diversity marketing, marketing communication targeting diverse customers * ...
and community structure have been suggested to influence disease dynamics through a hypothesis termed the ‘dilution effect’ (Ostfeld and Keesing 2000). For ''Ribeiroia ondatrae'', host species differences in susceptibility can influence infection patterns in multi-species communities (Johnson et al. 2008, Johnson and Hartson 2009). As a result, more diverse larval amphibian communities that include species with differing susceptibilities can alter parasite infection success and the resulting pathology in sensitive host species. For instance, larval toads (a sensitive species) raised experimentally alongside larval gray treefrogs (a resistant species) exhibited 37% less infection and fewer malformations (Johnson et al. 2008).


Parasite-induced malformations and amphibian conservation

Perhaps the most unexplored, complex and vital aspects of trematode-caused amphibian malformations are the population-level consequences. Do these parasites and the malformations they induce pose a conservation risk? While no direct evidence linking trematode deformities and amphibian population declines exists, there are legitimate reasons for concern (Johnson and McKenzie 2008). For instance, in multiple species of frogs and toads, laboratory studies show that even low levels of ''Ribeiroia'' infection can induce 30-95% mortality (see Johnson et al. 2010). Correspondingly, multi-year field studies show that in localities of high infection and malformations in metamorphosing frogs, <2% of amphibians returning to breed exhibit malformations, suggesting ''Ribeiroia'' infection and malformations have deleterious consequences for individual survival and fecundity (Johnson et al. 2001). In specific wetlands that have historically exhibited a high prevalence of infection and malformations, several amphibian species have notably declined or disappeared (see Johnson and McKenzie 2008 for review). In light of these data, and the increasing evidence that ''Ribeiroia'' infections are on the rise (Johnson and McKenzie 2008), it is prudent to treat ''Ribeiroia ondatrae'' as a threat to amphibian populations and diversity, particularly in combination with other stressors.


See also

* Ribeiroia ondatrae


References

* Bacon, J.P., Gray J.A. and L. Kitson (2006)
Status and conservation of the reptiles and amphibians of the Bermuda islands
Applied Herpetology 3: 323-344. * Basch, P.F., and R.F. Sturrock. 1969. Life history of ''Ribeiroia marini'' (Faust and Hoffman, 1934) comb. N. (Trematoda: Cathaemasiidae). Journal of Parasitology 55: 1180-1184. * Beaver, P.C. (1939)
The morphology and life history of Psilostomum ondatrae
Price 1931 (Trematoda: Psilostomatidae). Journal of Parasitology 25: 383-393. * Daszak P, Cunningham AA and Hyatt AD (2000). Wildlife ecology - Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287: 443-449. * Dobson, A. and J. Foufopoulos (2001)
Emerging infectious pathogens of wildlife
Philosophical Transactions of The Royal Society of London Series B-Biological Sciences 356: 1001-1012. * Gilliland, M.G. and P.M. Muzzall (2002)
Amphibians, trematodes, and deformities: an overview from southern Michigan
Comparative Parasitology 69: 81-85. * Hoppe DM (2000)
History of Minnesota frog abnormalities: do recent findings represent a new phenomenon?
- In: Kaiser, H. and Casper, G. S. (eds.), Investigating amphibian declines: proceedings of the 1998 Midwest conference on declining amphibians. University of Iowa Press, pp. 86–89. * Johnson, P. T. J. and S. R. Carpenter (2008). Influence of eutrophication on disease in aquatic ecosystems: patterns, processes, and predictions. Chapter 4 (pp. 71–99) in R. Ostfeld, F. Keesing and V. Eviner (eds.), Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton University Press. * Johnson, P. T. J. and J. M. Chase (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7: 521-526. * Johnson, P. T. J. and R. B. Hartson (2009). All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78: 191-201. * Johnson, P. T. J., Hartson, R. B., Larson, D. J. and D. R. Sutherland (2008). Linking biodiversity loss and disease emergence: amphibian community structure determines parasite transmission and pathology. Ecology Letters 11: 1017-1026. * Johnson, P.T.J., Preu, E.R., Sutherland, D.R., Romansic, J., Han, B., and A.R. Blaustein (2006). Adding infection to injury: Synergistic effects of predation and parasitism on salamander limb malformations. Ecology 87: 2227-2235. * Johnson, P.T.J., Lunde, K.B., Ritchie, E.G., and A.E. Launer (1999). The effect of trematode infection on amphibian limb development and survivorship. Science 284: 802-804. * Johnson, P.T.J., Lunde, K.B., Zelmer, D.A. and J.K. Werner (2003). Limb deformities as an emerging parasitic disease in amphibians: Evidence from museum specimens and resurvey data. Conservation Biology 17: 1724-1737. * Johnson P.T.J. and K.B. Lunde (2005). Parasite infection and limb malformations: A growing problem in amphibian conservation. - In: Lannoo, M. (ed.) Amphibian declines: the conservation status of United States species. University of California Press, pp. 124–138. * Johnson, P. T. J., Lunde, K. B., Ritchie, E. G., Reaser, J. K., and A. E. Launer (2001). Morphological abnormality patterns in a California amphibian community. Herpetologica 57: 336–352. * Johnson, P.T.J., Lunde, K.B., Thurman, E.M, Ritchie, E.G., Wray, S.N., Sutherland, D.R., et al. (2002). Parasite (''Ribeiroia ondatrae'') infection linked to amphibian malformations in the western United States. Ecological Monographs 72: 151-168. * Johnson, P. T. J. and V. J. McKenzie (2008). Effects of environmental change on helminth infections in amphibians: exploring the emergence of "Ribeiroia" and "Echinostoma" infections in North America. Chapter 11 in Fried, B. and R. Toledo, The Biology of Echinostomes, Springer. * Johnson, P. T. J., Reeves, M. K., Krest, S. K. and A. E. Pinkney (2010). A decade of deformities: advances in our understanding of amphibian malformations and their implications. In Sparling, Linder, Bishop, Krest (eds), Ecotoxicology of Amphibians and Reptiles, 2nd edition. SETAC Press, Pensacola FL * Johnson P.T.J., Sutherland, D.R., Kinsella, J.M., and K.B. Lunde (2004). Review of the Trematode Genus ''Ribeiroia'' (Psilostomidae): Ecology, Life History and Pathogenesis with Species Emphasis on the Amphibian Malformation Problem. Advances in Parasitology: 57: 191-253. * Kiesecker, J.M. 2002. Synergism between trematode infection and pesticide exposure: A link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences USA 99: 9900-9904. * Lannoo, M.J., Sutherland, D.R., Jones, P., Rosenberry, D., Klaver, R.W., Hoppe, D.M. et al. (2003). Multiple causes for the malformed frog phenomenon. In: Multiple Stressor Effects in Relation to Declining Amphibian Populations (eds Linder, G., Little, E., Krest, S. & Sparling, D.). ASTM STP 1443. American Society for Testing and Materials, West Conshoshocken, PA, pp. 233–262. * Ouellet, M. (2000). Amphibian deformities: current state of knowledge. - In: Sparling, D. W., Bishop, C. and Linder, G. (eds.), Ecotoxicology of amphibians and reptiles. Society for Environmental Toxicology and Chemistry, pp. 617–661. * Reeves, M.K., Dolph, C.L., Zimmer, H., Tjeerdema, R.S. and A.T. Kimberly (2008). Road Proximity increases risk of skeletal abnormalities in wood frogs from National Wildlife refuges in Alaska. Environmental Health Perspectives 116: 1008-1014. * Rohr, J. R., Schotthoefer, A. M., Raffel, T. R., Carrick, H. J., Halstead, N., Hoverman, J. T., Johnson, C. M., Johnson, L. B., Lieske, C., Piwoni, M. D., Schoff, P. K. and Beasley, V. R. (2008a). Agrochemicals increase trematode infections in a declining amphibian species. Nature 455: 1235–1239. * Rohr, J.R., Raffle, T.R., Sessions, S.K., and P.J. Hudson (2008b.). Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 18: 1743-1753. * Skelly, S.R. Bolden, L.K. Freidenburg, N.A. Freidenfelds and R. Levey (2007). ''Ribeiroia'' infection is not responsible for Vermont amphibian deformities. EcoHealth 4: 156-163. * Schotthoefer, A.M., Cole, R.A., and V.R. Beasley (2003). Relationship of tadpole stage to location of echinostoma cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89: 475-482. * Stopper, G.F., Hecker, L., Franssen, R.A. and S.K. Sessions (2002). How trematodes cause limb deformities in amphibians. Journal of Experimental Zoology 294: 252-263. * Sutherland, D.R. (2005) Parasites of North American Frogs. Amphibian Declines: The Conservation Status of United States Species (ed. M.J.Lannoo), pp. 109–123. University of California Press, Berkeley, California.


Notes

{{Taxonbar, from=Q3005043 Parasites of molluscs Psilostomatidae Trematode genera