Hind limb malformations in free-living northern leopard frogs (Rana pipiens) from Maine, Minnesota, and Vermont suggest multiple etiologies

Meteyer, Carol U.; Loeffler, Ivonne; Fallon, John F.; Converse, Kathryn A.; E, Green; Helgen, Judy C.; Kersten, Susan M.; Levey, Richard; Eaton-Poole, L; Burkhart, James G.

doi:10.1002/1096-9926(200009)62:3<151::aid-tera3>3.0.co;2-2

Cited by 79 publications

(60 citation statements)

References 27 publications

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“…It has been argued that the range of malformation phenotypes observed in nature far outweigh the different phenotypes produced by retinoids in laboratory studies. Furthermore, the most common RA-induced duplications observed in laboratory studies are proximal-axis duplications, which are not found in nature (Meteyer et al 2000;Sessions et al 1999). These previous findings were some of the reasons why RA involvement was dismissed and mechanical perturbation by the parasite has been the prevailing explanation.…”

Section: Discussioncontrasting

confidence: 85%

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

et al. 2011

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The widespread reports of malformed frogs have sparked interest worldwide to try and determine the causes of such malformations. Ribeiroia ondatrae is a digenetic trematode, which has been implicated as one such cause, as this parasite encysts within the developing tadpole hind limb bud and inguinal region causing dramatic limb malformations. Currently, the mechanisms involved in parasite-induced limb deformities remain unclear. We sought to investigate whether the level of retinoic acid (RA), a morphogenetic factor known to play a critical role in limb bud formation, is altered by the presence of R. ondatrae within the infected tadpole. Alteration of RA levels within the limb bud caused by the presence of the parasite may be achieved in three ways. First, metacercariae are actively secreting RA; second, cercariae, upon entering the limb/inguinal region, may release a large amount of RA; finally, the metacercariae may induce either an increase in the synthesis or a decrease in the degradation of the host's endogenous retinoic acid levels. Here, we show through high performance liquid chromatography and mass spectrometry that limb bud tissue of Lithobates sylvaticus, which has been parasitised, contains 70% more RA compared to the unparasitised control. Furthermore, parasites that have encysted within the limb buds appear to contain substantially less RA (56%) than the free swimming cercariae (defined as the infectious stage of the parasite). Taken together, these data illustrate for the first time that encystment of R. ondatrae leads to an increase in RA levels in the tadpole limb bud and may offer insight into the mechanisms involved in parasite-induced limb deformities.

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Section: Discussioncontrasting

confidence: 85%

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

et al. 2011

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“…In no case, did any tadpole have a malformation that could be associated with either parasites or chemical compounds (Meteyer, 2000;Meteyer et al, 2000).…”

Section: Methodsmentioning

confidence: 99%

Life in the Slow Lane: The Effect of Reduced Mobility on Tadpole Limb Development

Abdala¹,

Ponssa²

2011

The Anatomical Record

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Movement is thought to be a primary agent eliciting basic responses in the vertebrate body, such as the proper development of the musculoskeletal system. Embryos do not passively await hatching or birth but rather begin active movement very early on in their development. Most studies dealing with embryonic responses to changes in mobility have been performed in chickens or mammals. Herein, we investigate for the first time whether the embryos of organisms that are free-living during development demonstrate the same morphological responses to reduced mobility as embryos that undergo development in controlled environments such as in utero or in a shelled egg. We changed the viscosity of the environment in which free-living anuran tadpoles grow by rearing them in an agar medium. We thus increased the viscosity of the growth medium resulting in a decrease in larval movement. We predicted that a substantial increase in viscosity of the medium in which the larvae were reared would have at least two consequences: (1) a reduction of tadpole mobility and (2) a delayed onset of skeletogenesis thus producing shorter long bones. Our predictions were upheld and tadpoles reared in an agar medium remain immobile longer and showed a delayed onset of skeletogenesis compared with controls. We propose that the developmental responses to the same stimulus are similar throughout tetrapods, regardless of their developmental context (i.e., intrauterine, within an egg, or free-living). Anat Rec, 295:5-17, 2012. V V C 2011 Wiley Periodicals, Inc.

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“…Abnormal amphibians were photographically registered in order to avoid sampling the same individuals more than once (Donelly et al 1994). We diagnosed abnormalities following Meteyer et al (2000) on living adult individuals. Furthermore, in the case of Leptodactylus latrans, we also studied juveniles.…”

Section: Amphibian Surveymentioning

confidence: 95%

Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina

Agostini¹,

Kacoliris²,

Demetrio³

et al. 2013

Dis. Aquat. Org.

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The occurrence of abnormalities in amphibians has been reported in many populations, and its increase could be related to environmental pollution and habitat degradation. We evaluated the type and prevalence of abnormalities in 5 amphibian populations from agroecosystems with different degrees of agricultural disturbance (cultivated and reference areas). We detected 9 types of abnormalities, of which the most frequent were those occurring in limbs. The observed prevalence of abnormality in assessed populations from cultivated and reference areas was as follows: Rhinella fernandezae (37.1 and 10.2%, respectively), Leptodactylus latrans adults (28.1 and 9.2%) and juveniles (32.9 and 15.3%), and Hypsiboas pulchellus (11.6 and 2.8%). Scinax granulatus populations did not show abnormalities. Pseudis minuta, which was only detected in the reference area, exhibited a prevalence of 13.3%. For R. fernandezae, L. latrans, and H. pulchellus, generalized linear mixed models showed that prevalence of abnormalities was significantly higher (p < 0.05) in cultivated than in reference areas. L. latrans juveniles were more vulnerable to abnormalities than adults (p < 0.05). The presence of abnormalities in some species inhabiting different agroecosystems suggests that environmental stress factors might be responsible for their occurrence. While we detected pesticides (endosulfan, cypermethrin, and chlorpyrifos) and lower dissolved oxygen levels in ponds of the cultivated area, no data are currently available on how other factors, such as injuries from predators and parasite infections, vary by land use. Further research will be necessary to evaluate possible causes of abnormalities detected in the present study mainly in the context of factor interactions.KEY WORDS: Agricultural disturbance · Pesticide · Brachydactyly · Ectrodactyly · Scoliosis · Developmental abnormality · Teratogen Resale or republication not permitted without written consent of the publisherDis Aquat Org 104: [163][164][165][166][167][168][169][170][171] 2013 studied . Experimental and field evidence supports a causal association between the trematode Ribeiroia and limb malformations (Johnson et al. 2003, Johnson & Hartson 2009. Predators, such as leeches, fish, and odonate naiads, can cause the loss of an appendage and/or abnormalities during the regeneration process . Laboratory studies indicate that UV-B radiation and chemical contaminants, including pesticides used in agricultural practices, can cause malformations (Greulich & Pflugmacher 2003, Brunelli et al. 2009, Agostini et al. 2010), but to date field studies have not provided conclusive evidence (Lannoo 2008. Some of these factors are considered the cause of amphibian population decline and extinction reported on a global scale, although the relationship between amphibian malformations and population declines remains unclear (Blaustein et al. 2011). Some authors have discussed the necessity to assess and categorize different types of abnormalities and their prevalence considering life s...

show abstract

Hind limb malformations in free-living northern leopard frogs (Rana pipiens) from Maine, Minnesota, and Vermont suggest multiple etiologies

Cited by 79 publications

References 27 publications

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

Life in the Slow Lane: The Effect of Reduced Mobility on Tadpole Limb Development

Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina

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