Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama

Abstract

Amphibian populations around the world are experiencing unprecedented declines attributed to a chytrid fungal pathogen, Batrachochytrium dendrobatidis. Despite the severity of the crisis, quantitative analyses of the effects of the epidemic on amphibian abundance and diversity have been unavailable as a result of the lack of equivalent data collected before and following disease outbreak. We present a community-level assessment combining long-term field surveys and DNA barcode data describing changes in abundance and evolutionary diversity within the amphibian community of El Copé, Panama, following a disease epidemic and mass-mortality event. The epidemic reduced taxonomic, lineage, and phylogenetic diversity similarly. We discovered that 30 species were lost, including five undescribed species, representing 41% of total amphibian lineage diversity in El Copé. These extirpations represented 33% of the evolutionary history of amphibians within the community, and variation in the degree of population loss and decline among species was random with respect to the community phylogeny. Our approach provides a fast, economical, and informative analysis of loss in a community whether measured by species or phylogenetic diversity.

Fig. 1.

Bivariate graph of average pair-wise distances of the COI versus 16S gene fragments showing the barcode gap for sympatric samples representing the amphibian fauna of G. D. Omar Torrijos H. National Park, Panama. Gray zones indicate the gap in genetic distances between the most divergent intraspecific samples and the least divergent interspecific samples, as measured by K2P distances: 0.01163 versus 0.01397 for 16S, and 0.06026 versus 0.12107 for COI. The width of the 16S gap is defined by the intraspecific divergence within Cochranella euknemos (blue dots) versus the interspecific distance between C. euknemos and C. granulosa (red dots). The width of the COI gap is defined by the intraspecific divergence within Hyalinobatrachium colymbiphyllum (green dots) versus the interspecific distance between Pristimantis cruentus and P. aff. museosus (yellow dots). Silverstoneia nubicola lineage A versus lineage B (purple dots) is an intermediate case showing a divergence of 0.08611 at COI (dashed line). We count lineage B as a candidate species. To aid in visualization of the gap, the x axis was arbitrarily cut off at 0.08 divergence.

Fig. 2.

Community phylogeny of the amphibians of El Copé, Panama, study site. Maximum likelihood phylogeny constrained to match known amphibian relationships (Materials and Methods) and inferred from concatenated DNA sequences of the COI and 16S gene fragments from 300 samples representing all 63 named amphibian species plus 11 candidate species (labeled in purple) known from the study transects of approximately 4 km² established in Omar Torrijos National Park. Branch lengths made ultrametric using the MPL algorithm. Branches are color-coded by percent decline in relative abundance following the catastrophic decline caused by the arrival of B. dendrobatidis (5). Red branches indicate 100% decline in relative abundance (extirpated category). Orange branches indicate a decline of 85% to 99% (critical category). Black indicates less decline or an increase in relative abundance. Taxonomic families of amphibians are indicated by brown circles: A, Aromobatidae; B, Bufonidae; C, Caecilidae (a caecilian); Ce, Centrolenidae; Cr, Craugastoridae; D, Dendrobatidae; E, Eleutherodactylidae; H1–H3, Hylidae (H2, Phyllomedusinae); He, Hemiphractidae; Le, Leptodactylidae; Li, Leiuperidae; M, Microhylidae; P, Plethodontidae (salamanders); R, Ranidae; and S, Strabomantidae.