Amphibian diversity: decimation by disease.
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Amphibians↗
Biomedical subjects
Pieter T J Johnson
Publications and source records attributed to Pieter T J Johnson.
Dining on disease: how interactions between infection and environment affect predation risk.
Despite growing interest in ecological interactions between predators and pathogens, few studies have experimentally examined the consequences of infection for host predation risk or how environmental conditions affect this relationship. Here we combined mesocosm experiments, in situ foraging data, and broad-scale lake surveys to evaluate (1) the effects of chytrid infection (Polycaryum laeve) on susceptibility of Daphnia to fish predators and (2) how environmental characteristics moderate the strength of this interaction. In mesocosms, bluegill preferred infected Daphnia 2-5 times over uninfected individuals. Among infected Daphnia, infection intensity was a positive predictor of predation risk, whereas carapace size and fecundity increased predation on uninfected individuals. Wild-caught yellow perch and bluegill from in situ foraging trials exhibited strong selectivity for infected Daphnia (3-10 times over uninfected individuals). In mesocosms containing water high in dissolved organic carbon (DOC), however, selective predation on infected Daphnia was eliminated. Correspondingly, lakes that supported chytrid infections had higher DOC levels and lower light penetration. Our results emphasize the strength of interactions between parasitism and predation while highlighting the moderating influence of water color. P. laeve increases the conspicuousness and predation risk of Daphnia; as a result, infected Daphnia occur predominantly in environments with characteristics that conceal their elevated visibility.
Animals↗
Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations.
We explored the importance of interactions between parasite infection and predation in driving an emerging phenomenon of conservation importance: amphibian limb malformations. We suggest that injury resulting from intraspecific predation in combination with trematode infection contributes to the frequency and severity of malformations in salamanders. By integrating field surveys and experiments, we evaluated the individual and combined effects of conspecific attack and parasite (Ribeiroia ondatrae) infection on limb development of long-toed salamanders (Ambystoma macrodactylum). In the absence of Ribeiroia, abnormalities involved missing digits, feet, or limbs and were similar to those produced by cannibalistic attack in experimental trials. At field sites that supported Ribeiroia, malformations were dominated by extra limbs and digits. Correspondingly, laboratory exposure of larval salamanders to Ribeiroia cercariae over a 30-day period induced high frequencies of malformations, including extra digits, extra limbs, cutaneous fusion, and micromelia. However, salamander limbs exposed to both injury and infection exhibited 3-5 times more abnormalities than those exposed to either factor alone. Infection also caused significant delays in limb regeneration and time-to-metamorphosis. Taken together, these results help to explain malformation patterns observed in natural salamander populations while emphasizing the importance of interactions between parasitism and predation in driving disease.
Ambystoma↗
In vitro excystment of the metacercariae of Ribeiroia ondatrae.
In vitro excystation studies were done on the metacercarial cysts of Ribeiroia ondatrae obtained from naturally infected leopard frogs, Rana pipiens. Studies were done in Petri dish cultures in various media maintained at 41 degrees C. The media consisted of 0.5% trypsin-0.5% bile salts in Earle's balanced salt solution at pH 7.8 (TB), 1% acid pepsin (AP) in 0.85% saline adjusted to pH 2 with HCl; acid saline (AS) adjusted to pH 2 with HCl, and saline (S). The TB medium, used successfully to excyst the metacercariae of numerous species of digeneans, did not induce excystation of Ribeiroia ondatrae. Some excystation occurred in AS but not in S. Excystation was 100% in AP with most organisms excysting within 30 s after placement in the medium at 41 degrees C. Excystation in vitro in AP at 41 degrees C is compatible with the fact that this organism establishes itself in the acid-pepsin environment of the proventriculus of avian hosts.
Animals↗
A molecular phylogenetic study of the genus Ribeiroia (Digenea): trematodes known to cause limb malformations in amphibians.
Species of Ribeiroia (Trematoda: Psilostomidae) are known to cause severe limb malformations and elevated mortality in amphibians. However, little is known regarding the number of species in this genus or its relation to other taxa. Species of Ribeiroia have historically been differentiated by slight differences among their larval stages. To better understand the systematics and biogeography of this genus and their potential relevance to the distribution of malformed amphibians, specimens identified as Ribeiroia were collected across much of the known range, including samples from 5 states in the United States (8 sites) and 2 islands in the Caribbean (Puerto Rico and Guadeloupe). A cercaria from East Africa identified as Cercaria lileta (Fain, 1953), with attributes suggestive of Ribeiroia (possibly R. congolensis), was also examined. The intertranscribed spacer region 2 (ITS-2) of the ribosomal gene complex was sequenced and found to consist of 429 nucleotides (nt) for R. ondatrae (United States) and 427 nt for R. marini (Caribbean), with only 6 base differences noted between the 2 species. The ITS-2 region of C. lileta (429 nt) aligned closely with those of the 2 other Ribeiroia species in a phylogenetic analysis that included related trematode genera. This evidence suggests that a third Ribeiroia species exists in tropical Africa. Variation in ITS-2 within R. ondatrae was nonexistent among the 8 populations from North America. Our study further suggests that Ribeiroia spp. originally parasitized Biomphalaria sp., and that a host switch to a closely related snail, Helisoma sp., may have occurred in the lineage represented by R. ondatrae. However, relationships within the Echinostomatidae are not understood well enough to make any robust conclusions at this time.
Amphibians↗
Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem.
Trematodes in the genus Ribeiroia have an indirect life cycle involving planorbid snails as first intermediate hosts, fishes or amphibians as second intermediate hosts and birds or mammals as definitive hosts. Although rarely pathogenic in definitive hosts, Ribeiroia infection can cause severe pathology and mortality in snails and amphibians. This group of parasites has gained notoriety for its prominent rol in the recent rash of amphibian deformities in North America. Under some circumstances, these malformations may enhance parasite transmission by rendering infected amphibian hosts more susceptible to definitive host predators. However, increasing reports of malformations in North American amphibian populations emphasize the importance of understanding infection patterns. Here we review important aspects of the biology, ecology, life cycle and pathogenesis of parasites in the genus Ribeiroia and identify priorities for future research. Based on available morphological descriptions and preliminary molecular data, three species of Ribeiroia are recognized: R. ondatrae in the Americas, R. marini in the Caribbean and R. congolensis/C. lileta in Africa. We further evaluate the influence of abiotic and biotic factors in determining the intensity and prevalence of Ribeiroia infection and malformations in amphibians, highlighting the importance of habitat alteration and secondary factors (e.g. aquatic eutrophication, contaminants) in promoting infection. Although not a "new" parasite, Ribeiroia may have increased in range, prevalence, or intensity in recent years, particularly within amphibian hosts. Nevertheless, while much is known about this intriguing group of parasites, there remains much that we do not know. Particular importance for future research is placed on the following areas: evaluating the phylogenetic position of the genus, establishing the molecular mechanism of parasite-induced malformations in amphibians, isolating the drivers of parasite transmission under field conditions and studying the consequences of malformations for parasite and host populations. Investigation of these questions will benefit enormously from a multidisciplinary approach that effectively integrates parasitology, developmental biology, immunology, herpetology and aquatic ecology.
Amphibians↗
Amphibian deformities and Ribeiroia infection: an emerging helminthiasis.
Since their widespread appearance in the mid-1990s, malformed amphibians have evoked fear, as well as fascination within the scientific and public communities. Recent evidence from field and laboratory studies has implicated infection by a digenetic trematode--Ribeiroia ondatrae--as an important cause of such deformities. Ribeiroia spp. have a complex life cycle involving planorbid snails, amphibians and water birds. Under natural conditions, malformations might promote parasite transmission by increasing the susceptibility of infected amphibians to predation by definitive hosts. However, with respect to the recent outbreak of deformities, we suggest that exogenous agents (e.g. pesticides, nutrient run-off, introduced fishes) might be interacting with Ribeiroia, resulting in elevated infection levels, and we highlight the need for studies incorporating multiple stressor dynamics to further explore this problem.
Amphibians↗
Explaining frog deformities.
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Amphibians↗