Limb Deformities as an Emerging Parasitic Disease in Amphibians: Evidence from Museum Specimens and Resurvey Data

: Widespread reports of malformed amphibians are of growing conservation concern. Although accounts of mass malformations (>5%) in North American amphibian populations date back to the 1940s, they are often poorly documented and are rarely explained. We reviewed available information for nine historical accounts from California, Colorado, Idaho, Mississippi, Montana, Ohio, and Texas reported between 1946 and 1988. We then asked the following questions: (1) Which of these cases were associated with Ribeiroia (Trematoda: Digenea) infection? (2) Are malformations still occurring at these sites? And (3) if so, have the frequency or types of abnormalities changed? Each site was resurveyed between 1999 and 2002, and original voucher specimens were redescribed and examined for trematode infection. Direct identification and classification by discriminant function analysis indicated that historical malformations at six of eight sites were associated with infection by Ribeiroia, dating back as far as 1946. Malformations recorded historically at these sites were consistent with the documented effects of Ribeiroia infection, including extra limbs, cutaneous fusion, and bony triangles. Of the six sites that still supported amphibians upon resurvey, three continued to support severe limb malformations at frequencies of 7–50% in one or more species. Although no pesticides were detected, amphibians from each of these sites were infected with Ribeiroia metacercariae. Taken together, these results suggest that Ribeiroia infection has historically been an important cause of mass malformations in amphibians. We conclude that although parasite-induced malformations are not a new phenomenon, there is qualitative evidence suggesting that their prevalence has increased recently, and we highlight the need for long-term research to evaluate the impacts of malformations on amphibian population viability. Resumen: Los informes generalizados de anfibios malformados son motivo de creciente preocupacion para la conservacion. Aunque los registros de malformaciones masivas (>5%) en poblaciones de anfibios de Norte America datan de 1940, a menudo estan escasamente documentados y rara vez explicados. Revisamos la informacion disponible para nueve informes historicos de California, Colorado, Idaho, Mississippi, Montana, Ohio y Texas entre 1946 y 1988. Posteriormente preguntamos: (1) ?Cuales de estos casos estaban asociados con la infeccion de Ribeiroia (Trematoda: Digenea)? (2) ?Aun ocurren malformaciones en estos sitios? y (3) Si es asi, ?ha cambiado la frecuencia o tipos de anormalidades? Cada sitio fue muestreado de nuevo entre 1999 y 2002 y los especimenes originales fueron descritos y examinados nuevamente para ver si tenian infeccion de trematodos. La identificacion directa y la clasificacion por analisis discriminante indicaron que las malformaciones historicas en seis de los ocho sitios estaban asociadas con infeccion por Ribeiroia, que data desde 1946. Las malformaciones registradas historicamente en estos sitios fueron consistentes con los efectos documentados de infeccion de Ribeiroia, incluyendo extremidades adicionales, fusion cutanea y triangulos oseos. De los seis sitios donde aun habia anfibios en los muestreos recientes, tres todavia presentaban malformaciones severas de las extremidades con frecuencias del 7 al 50% en una o mas especies. Aunque no se detectaron pesticidas, los anfibios de cada uno de estos sitios estaban infectados con metacercarias de Ribeiroia. En conjunto, estos resultados sugieren que la infeccion por Ribeiroia historicamente ha sido una causa importante de malformaciones masivas en anfibios. Concluimos que, aunque las malformaciones inducidas por parasitos no son un fenomeno nuevo, existe evidencia cualitativa que sugiere que su prevalencia ha incrementado recientemente, y destacamos la necesidad de investigacion a largo plazo para evaluar los impactos de malformaciones sobre la viabilidad de poblaciones de anfibios.