Tests of Null Models for Amphibian Declines on a Tropical Mountain

Abstract

Many of the recent, widespread declines and disappearances of amphibian populations have taken place in seemingly undisturbed, montane habitats. The question of whether the observed patterns differ from those expected from natural population dynamics is the subject of an ongoing controversy with important implications for conservation. We examined this issue for the Monteverde region of Costa Rica’s Cordillera de Tilarán, where a multi‐species population crash in 1987 led to the disappearance of the endemic golden toad ( Bufo periglenes) and many other species. Focusing on long‐term studies of other amphibian assemblages, we developed probabilistic null models for the number of disappearances. Tests of these models at Monteverde suggest that the patterns observed there are highly improbable in the context of normal demographic variability. Twenty species of frogs and toads (40% of the anuran fauna) were missing throughout our 1990–1994 surveys of a 30‐km2 area. Not all organisms in this area had declined accordingly: the relative frequency of absences was much greater for anurans than for breeding birds. Nevertheless, anuran habitats, most of which are protected within the Monteverde Cloud Forest Preserve, seemed unchanged, and none of the breeding‐bird species known to be sensitive to deforestation was missing. Thus, only factors other than direct, obvious human impacts can explain the amphibian declines. Consistent with our tests of null models, analyses of recent population trends do not support the hypothesis that the 1987 crash was an extreme fluctuation from which populations are recovering. Surviving species for which baseline data are available—stream‐breeding glass frogs ( Hyalinobatrachium fleischmanni and Centrolenella prosoblepon) and a pond‐breeding treefrog ( Hyla pseudopuma)—remained far less abundant than they were before the crash and showed no increase during 1990‐1994. We documented an increase only for one terrestrial‐breeding rain frog ( Eleutherodactylus diastema).Pruebas de Modelos Nulos para Disminuciones de Anfibios en una Montaña TropicalMuchas de las disminuciones y desapariciones recientes de poblaciones de anfibios en varias partes del mundo se han producido en hábitats que aparentemente no han sido alterados. La pregunta de si los patrones observados difieren de lo que es predicho por la dinámica natural de poblaciones es el tema de una controversia actual que tiene consecuencias importantes para la conservación. Se examinó esta pregunta para la región de Monteverde en la Cordillera de Tilarán, Costa Rica, donde un colapso de poblaciones en 1987 produjo la desaparición del endémico sapo dorado ( Bufo periglenes) y muchas otras especies. Centrándose en estudios a largo plazo sobre anfibios de otras regiones, se desarrollaron modelos nulos probabilísticos con respecto al número de desapariciones. Al probarse estos modelos para Monteverde se sugiere que los patrones observados son poco probables dentro de los parámetros normales de la variabilidad demográfica. Durante 1990‐1994 en un área de 30‐km2, veinte especies de ranas y sapos (el 40% de los anuros de la región) estuvieron ausentes. No todos los organismos del área disminuyeron de la misma forma: por ejemplo, la frecuencia relativa de especies ausentes fue mucho mayor para los anuros que para las aves que se reproducen en el área de estudio. Sin embargo, la mayoría de los hábitats de anuros están protegidos dentro de la Reserva Biológica Bosque Nuboso de Monteverde, y no parecía que habían cambiado. Además, ninguna de las especies de aves que son afectadas de manera negativa por la deforestación estuvo ausente. Por lo tanto, las disminuciones de anfibios sólo pueden ser explicadas por factores que no son los impactos obvios y directos causados por los seres humanos. De acuerdo con nuestras pruebas de modelos nulos, los análisis de tendencias recientes de abundancia no apoyan la hipótesis de que el colapso de 1987 fuera una fluctuación extrema de la cual las poblaciones están recuperándose. Las especies sobrevivientes de las que existen datos demográficos anteriores al colapso—ranas de vidrio ( Hyalinobatrachium fleischmanni y Centrolenella prosoblepon), que se reproducen en quebradas, y una rana arborícola ( Hyla pseudopuma) que pone huevos en lagunas y pozos—eran mucho menos abundantes durante 1990–1994 de lo que fueron antes de este evento y no se encontró evidencias de aumento. Se documentó un incremento solo en las poblaciones de Eleutherodactylus diastema, que se reproduce en hábitats terrestres.

Tropical cloud forest climate variability and the demise of the Monteverde golden toad

“…The decline of amphibians in El Yunque Forest in Puerto Rico is believed to be a consequence of a change in their behavior during dry periods, with populations moving from a dispersed distribution to a few protected microsites on the landscape, increasing their vulnerability to contagion (48). Similar patterns were observed at Monteverde prior to the multispecies population crash and extinction of the golden toad in 1987 (1,9,34,41). Extinction events are an omnipresent feature of the history of life (49).…”

“…In that case, warmer Pacific SSTs were interpreted to correspond to warmer, drier conditions in the cloud forest. Based on statistical hypothesis testing, Pounds and coauthors (34) subsequently concluded that the abnormal dry conditions of 1987 were likely to have caused the multispecies population crash, which included the extinction of the Monteverde Golden Toad. Both of these papers speculated at the time that disease may have been the proximate cause of the extinction of the golden toad (9, 34).…”

“…It is possible that Batrachochytrium dendrobatidis was already present in Monteverde prior to that year (40). Dry conditions culminating during the reproductive season in 1987 would have caused amphibian populations to coalesce around a few remaining wet microhabitats (1,34,41), where the fungus would have been able to spread rapidly through the population and ultimately result in extinction.…”

Predicted Disease Susceptibility in a Panamanian Amphibian Assemblage Based on Skin Peptide Defenses

“…Although it is not the only agent of declines in this region, the southeastward spread of chytridiomycosis is depleting amphibian populations (Daszak et al, 2003;Lips et al, 2003a). Monitored populations have declined throughout Costa Rica (Pounds et al, 1997; and western Panama, and chytridiomycosis was associated with these events (Berger et al, 1998;Lips, 1999;Lips et al, 2003a).…”

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

“…In Central America, the decimation of highland amphibian populations was first noted in Monteverde, Costa Rica (35,36), in the late 1980s, and since then the spread of B. dendrobatidis has been moving in an epidemic wave from the northwest toward the southeast through the cordillera of Isthmian Central America (9,(37)(38)(39)(40). Anticipating the arrival of B. dendrobatidis, an intensive field survey and monitoring program was established in 1998 in the G. D. Omar Torrijos H. National Park (latitude 08.667, longitude −080.592) at 800 m elevation, near El Copé, Panama (9).…”