Ribeiroia

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Ribeiroia
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Platyhelminthes
Class: Trematoda
Order: Plagiorchiida
Family: Psilostomatidae
Genus: Ribeiroia
Travassos, 1939
Type species
Ribeiroia insignis
Travassos, 1939[1]
= Ribeiroia ondatrae (Price, 1931)
Species

Ribeiroia congolensis
Ribeiroia marini
Ribeiroia ondatrae

Ribeiroia (

mammals as definitive hosts (see § Life history). In North America, infection by Ribeiroia has been linked to amphibians with limb malformations. The connection between parasitic infection and limb malformations has generated questions about (a) whether parasite-induced malformations in amphibians are increasing (see § Evidence for emergence), and (b) the consequences of such abnormalities for amphibian population conservation (see § Parasite-induced malformations and amphibian conservation
).

Taxonomy

Ribeiroia is a genus of parasites in the class

Cladocystis trifolium, Cathemasia, and Echinostoma (Johnson et al. 2004). See Johnson et al. (2004) for more details on morphological and ecological differences as well as phylogenetic
relationships between these species.

Life cycle

Ribeiroia ondatrae has an indirect complex

parasite stage with a thin outer membrane. 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 of birds and the stomach of mammals.[4]

Infection and amphibian malformations

Pacific tree frog with limb malformation induced by Ribeiroia ondatrae

Laboratory studies

Experimental exposure to Ribeiroia ondatrae cercariae has been shown to cause limb malformations in various frog, toad and

teratogenic chemical by parasites, or a combination of the two.[7]

Susceptibility to infection and the subsequent pathology differs among amphibian species. For example,

Hyla versicolor) 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), supernumerary limbs and digits (polymelia and polydactyly
), 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 and midwestern US.[8] 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.[9] 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,[10] but it was not detected in malformation surveys from Vermont, Alaska, Bermuda, and Michigan.[11]

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 flyways, with concentrations along the Pacific, Mississippi, and Atlantic 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 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 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:

  1. a wider range of more severe malformations,
  2. a greater number of affected amphibian species,
  3. a larger number of affected sites, and
  4. 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 and phosphorus enrichment are widespread forms of anthropogenic environmental change that may influence parasite infection (Johnson and Carpenter 2008). Nutrient enrichment leads to eutrophication, which has been linked with emergence of Ribeiroia ondatrae through direct and indirect effects on aquatic food webs (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 - Pesticides 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 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

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

References

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  • 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.
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  • 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.
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  • 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.
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Notes

  1. ^ Travassos, L. (1939). "Um novo trematódeo parasite da garças: Ribeiroia insignia n. g., n. sp. Anexo N. 3 ao Relatório da excursäo científica do Instituto Oswaldo Cruz realizada na zona da E. F. N. O. B., em outubro de 1938". Boletim Biológico (in Portuguese). 4: 301–304.
  2. ^ Beaver 1939; Basch and Sturrock 1969; Johnson et al. 2004
  3. ^ Beaver 1939; Basch and Sturrock 1969; Johnson et al. 2004
  4. ^ Johnson et al. 2004
  5. ^ Johnson et al. 1999; 2001; 2006; Stopper et al. 2002; Schotthoefer et al. 2003; Johnson and Hartson 2009
  6. ^ Schotthoefer et al. 2003
  7. ^ Johnson et al. 1999; Stopper et al. 2002
  8. ^ reviewed in Johnson et al. 2010
  9. ^ Johnson et al. 2002
  10. ^ Kiesecker 2002; Lannoo et al. 2003; Sutherland 2005; Johnson and Hartson 2009
  11. ^ Gilliland and Muzzall 2002; Bacon et al. 2006; Skelly et al. 2007; Reeves et al. 2008