Amphibian Deformities and Disease


What’s Wrong With Our Frogs?

Our group uses parasite-induced malformations in amphibians as a model system to investigate how environmental change affects the levels of disease pathology.  Currently we seek to understand how different forms of environmental change, including pollution (e.g., nutrient and pesticide runoff), climate change, and biodiversity loss, affect parasite abundance and the frequency of malformations.  An additional yet no less important priority is to identify the consequences of such pathology for amphibian population persistence.


History

Beginning around the mid-1990s, numerous reports of malformed amphibians generated widespread concern among scientists, health officials, and state and federal agencies. In large part, these malformations involved limb deformities in recently metamorphosed frogs. Extra limbs, partially and completely missing limbs, and a variety of other limb malformations (e.g., skin webbings, bony triangles) comprised many of the observed deformities (malformation gallery). In the United States, concentrations of hotspots have been reported in the western US, the Midwest, and the Northeast (including parts of southern Canada). Concern over possible threats to human health and ongoing declines in amphibian populations prompted intensive research by a variety of academic and government organizations. Broadly, research has focused on the following potential causes: chemical contamination (including retinoids and endocrine disruptors), UV-B radiation, sublethal predation, and parasite infection. For a recent review, see Johnson et al. (2010). This issue is still very much alive, and new malformations sites continue to be discovered each and every year (www.deformedfrogs.org).

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A Fluke of Nature

Research in our lab has focused on trematode parasite infection, which has been implicated as an important cause of malformations in amphibians across North America. Specifically, the digenetic trematode Ribeiroia ondatrae has been closely linked to the occurrence of severe limb deformities in amphibians both in experimental studies as well as large-scale field surveys involving thousands of examined animals. It is a particularly prevalent cause of limb deformities in the western United States, including California, Oregon, Washington, and Montana, although the parasite has been detected across much of the USA. Although the types of deformities induced vary by amphibian species, Ribeiroia has been shown to cause extra limbs (up to 6 extra limbs or 10 limbs total), partially and completely missing limbs, bony triangles, skin webbings, and digit alterations (see here for images of deformities). Based on laboratory trials, mark-release-recapture studies, and multi-year surveys, frogs with parasite-induced deformities are less able to jump, swim, obtain food, or survive to maturity, even following years in which a large fraction of emerging frogs are malformed.

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Trematode Parasite Infection

Digenetic trematodes, such as Ribeiroia ondatrae, are parasitic flatworms with complex life cycles, typically involving two or more hosts. Species in the genus Ribeiroia utilize three hosts: rams horn snails, larval amphibians or fishes, and birds or mammals. Snails function as the first intermediate hosts, in which the parasite undergoes asexual reproduction to produce free-swimming cercariae. Cercariae encyst around the developing limbs of larval amphibians, wherein they form a resting stage (metacercariae) that can interfere with proper limb development. For the parasite to complete its life cycle, an infected amphibian must be consumed by a suitable definitive host. Definitive hosts for Ribeiroia are typically birds, such as herons, raptors, or waterfowl within which the adult parasite reproduces sexually and releases eggs in the host feces. Eggs hatch in water, releasing free-swimming miracidia that infect snails, continuing the cycle. Perhaps most disturbingly, malformations caused by Ribeiroia are hypothesized to increase the susceptibility of infected frogs to predation, potentially enhancing parasite transmission between its second intermediate (amphibians) and definitive hosts (birds). A variety of other parasites with complex life cycles are known to alter either the appearance or behavior of their second intermediate hosts, effectively rendering them more vulnerable to predatory definitive hosts.

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Deformities and Amphibian Conservation

A final yet pressing priority in the study of amphibian malformations is to identify the long-term consequences of Ribeiroia infection and malformations for amphibian population persistence.  Malformed frogs do not survive to sexual maturity, likely succumbing to predators and/or starvation, and Ribeiroia infection itself is highly lethal to amphibian larvae. Deformities have also been reported in a number of threatened or endangered amphibians, such as the California red-legged frog. Considering that malformations can affect >50% of the emerging frogs in a population, the net effects of infection and malformations on mortality may be substantial. Although anecdotal reports have linked malformations and amphibian declines in select populations, there have been no attempts to quantify the effects of Ribeiroia relative to other sources of mortality, particularly under field conditions. This is a key issue toward evaluating the conservation significance of amphibian malformations.  


Project Publications  

Huver, J. R., Koprivnikar, J., Johnson, P. T. J. and S. Whyard (2015). Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. Ecological Applications 25: 991–1002. pdf_icon small.gif

Reeves, M., Medley, K., Pinkney, A., Holyoak, M., Johnson, P. T. J. and M. Lannoo (2013). Localized hotspots drive continental geography of abnormal amphibians. PLoS ONE 8: e77467. doi:10.1371/journal.pone.0077467 

Johnson, P. T. J., Preston, D. L., Hoverman, J. T., and K. L. D. Richgels (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494: 230-234. pdf_icon small.gif

Lunde, K. B., Resh, V. T, and P. T. J. Johnson (2012). Using an ecosystem-level manipulation to understand host-parasite interactions and how they vary with study venue. Ecosphere 3: 84. pdf_icon small.gif

Lunde, K. B. and P. T. J. Johnson (2012). A practical guide for the study of malformed amphibians and their causes. Journal of Herpetology 46: 429-441. pdf_icon small.gif

Goodman, B. A. and P. T. J. Johnson (2011). Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PLoS ONE 6: e20193. pdf_icon small.gif

Johnson, P. T. J. and J. Bowerman (2010). Do predators cause frog deformities? The need for an eco-epidemiological approach.  Journal of Experimental Zoology 314B: 515-518. pdf_icon small.gif

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. Chapter 16 (pp. 511-536) In D. W. Sparling, G. Linder, C. A. Bishop, and S. K. Krest (eds), Ecotoxicology of Amphibians and Reptiles, 2nd edition.  SETAC Press, Pensacola FL. 


In the Press

“World’s Weirdest Events”: in this new television show, the Johnson’s Lab research on parasite-induced deformities in amphibians is featured in episode 6, including footage of field and laboratory work as well as a sit-down interview with Dr. Johnson. Watch here.

“The Life Parasitic”: in a March 2015 interview with the BBC series The Naked Scientists, Dr. Johnson discusses the ways in which parasites can hijack their hosts to meet their own reproductive ends. Listen to the podcast here.

“Mind suckers: meet nature’s nightmare”: in the November 2014 issue of National Geographic, the cover story focuses on the capacity of parasites to alter their hosts in bizarre yet fascinating ways. The accompanying story by Carl Zimmer features a broad range of examples, including the ability of the trematode parasite Ribeiroia ondatrae to cause severe deformities in frogs. The story includes photos from the Johnson Lab and a graphic novel of the Ribeiroia life cycle developed in collaboration with our lab. See full cover story here.

Altered amphibians”: High County News highlights efforts of the Johnson Lab to understand the drivers and consequences of malformed amphibians. Includes a news article and photo log.

“Parasites creating deformed frogs in western US”: National Geographic News covers recent (2011) efforts by the Johnson Lab, including work by graduate student Sara Paull, in re-surveying amphibian malformation sites across the western United States. This work shows a link to parasitism and explores the implications of this disturbing phenomenon. Click for the full story or photo log.

“Researchers battle parasite-driven frog deformities”: A 2011 story featured on PBS details efforts by our group to explore methods that can help reduce infections and promote amphibian conservation. See feature here.


Project Links

Have You Found a Deformed Frog? Report it here

Malformation Nation: a citizen science website for frog deformities

Aquatic Parasite Observatory: learn about parasites found in frogs, fishes, and other aquatic hosts

Informational brochure about deformed amphibians [pdf]

Freshwaters Illustrated: images of deformed amphibians and ongoing research