Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain

Abstract

During the summers of 1997, 1998 and 1999 mass mortality episodes of post-metamorphic common midwife toads (Alytes obstetricans) occurred in a protected area in central Spain. The population suffered a sharp decline, disappearing from 86% of the ponds where they were known to reproduce some years ago. Scanning electron microscopy and histological techniques revealed the presence of a chytridiomycosis infection in the skin of the toads. This evidence supports chytridiomycosis as the most plausible cause of the decline of the species in the area. This is the first report of an apparent chytridium-caused amphibian decline in Europe.

Introduction

Declines of amphibian populations in their natural habitats, with no identifiable direct causes, have become a subject of increasing concern for the scientific community in recent years (Blaustein and Wake, 1990, Wake, 1991, Blaustein, 1994, McCoy, 1994). It is a complex problem with multiple potential causes whose relative importance in local extinction processes has yet to be established, as well as the extent to which these factors affect normal population dynamics of amphibians (Pechman et al., 1991, Alford and Richards, 1999). Several studies have provided solid evidence of disappearances of populations that were common only a few decades ago, particularly in montane, well conserved habitats (Bradford, 1991, Carey, 1993, Richards et al., 1993, Lips, 1998). Some of these studies have implicated abiotic agents in the declines, mostly physical changes in the environment which act as stressing factors affecting normal physiological functions of the amphibians (Bradford et al., 1992, Blaustein et al., 1994). Biotic factors have also been implicated in some cases, as in the recent description of a pathogenic fungus which has been causally related to amphibian population declines in Australia and Northern, Central and South America (Berger et al., 1998, Daszak et al., 1999, Pessier et al., 1999). This fungus belongs to the order Chytridiales, and has been included in a new genus, Batrachochytrium (Longcore et al., 1999). It is waterborne and pathogenic to adult amphibians, although it does not kill tadpoles; it prefers cooler temperatures, and is not solely dependent upon the highly susceptible host species for its continued existence (Berger et al., 1999a). Chytrids were not known to parasitise vertebrates prior to these studies.

Chytridiomycosis is a fatal disease which has been identified in an increasing number of amphibian species, as preserved material from populations affected some years ago is being re-studied. The disease can be carried by healthy tadpoles and has also been found in a small proportion of apparently healthy frogs and tadpoles (Berger et al., 1999a). In post-metamorphic amphibians it causes a widespread infection of the skin, resulting in hyperkeratosis, sloughing and erosions of the epidermis, and occasional ulcerations (Berger et al., 1999a).

No fungal infections causing amphibian declines have been reported so far in Europe, and such declines have mainly occurred as a result of conventional reasons associated with habitat loss and disturbance (e.g. Cooke, 1972, Beebee, 1977, Kuzmin, 1994, Cunningham et al., 1996). Unlike other parts of the world, no species in Europe has gone extinct recently, and the cases of apparently inexplicable declines are very unusual (e.g. Semb-Johansson, 1992).

In Spain, a recent case was observed in July 1992 and 1994, when two episodes of mass mortality of larval and metamorphic common midwife toads (Alytes obstetricans) were recorded in a lake in the Pyrenean Mountains (Márquez et al., 1995). In that case, the bacterium Aeromonas hydrophila, which produces a disease commonly known as “red leg”, was shown to be responsible for the mortality.

In the summers of 1997 and 1998, thousands of dead, post-metamorphic A. obstetricans were found around the ponds in the Peñalara Natural Park in central Spain. They had an apparently healthy general aspect, showing no traces of red-leg infection. Dead tadpoles or adults were not found. A limnological study was performed during the summer of 1998 in which 25 water chemistry variables were measured in selected ponds, and a rare increase in pH (up to 9) in some of the ponds was reported (Toro and Granados, personal communication). In the summer of 1999 we carried out a study of the A. obstetricans population to detect the potential causes of the mass mortality in order to act as soon as possible to ensure the conservation of the populations, which are isolated from other populations in central Spain (Garcı́a-Parı́s, 1995).