Luis A. Coloma

Widespread amphibian extinctions from epidemic disease driven by global warming

As the Earth warms, many species are likely to disappear, often because of changing disease dynamics. Here we show that a recent mass extinction associated with pathogen outbreaks is tied to global warming. Seventeen years ago, in the mountains of Costa Rica, the Monteverde harlequin frog (Atelopus sp.) vanished along with the golden toad (Bufo periglenes). An estimated 67% of the 110 or so species of Atelopus, which are endemic to the American tropics, have met the same fate, and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) is implicated. Analysing the timing of losses in relation to changes in sea surface and air temperatures, we conclude with ‘very high confidence’ (> 99%, following the Intergovernmental Panel on Climate Change, IPCC) that large-scale warming is a key factor in the disappearances. We propose that temperatures at many highland localities are shifting towards the growth optimum of Batrachochytrium, thus encouraging outbreaks. With climate change promoting infectious disease and eroding biodiversity, the urgency of reducing greenhouse-gas concentrations is now undeniable.

Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages

The Neotropics contains half of remaining rainforests and Earths largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.

Multiple, recurring origins of aposematism and diet specialization in poison frogs

Aposematism is the association, in a prey organism, of the presence of a warning signal with unprofitability to predators. The origin of aposematism is puzzling, because of its predicted low probability of establishment in a population due to the preys increased conspicuousness. Aposematism is a widespread trait in invertebrate taxa, but, in vertebrates, it is mostly evident in amphibians, reptiles, and fishes. Poison frogs (Dendrobatidae) are one of the most well known examples of the co-occurrence of warning coloration and toxicity. This monophyletic group of mostly diurnal leaf-litter Neotropical anurans has both toxic/colorful and palatable/cryptic species. Previous studies suggested a single origin of toxicity and warning coloration, dividing the family in two discrete groups of primitively cryptic and more derived aposematic frogs. Recent molecular phylogenetic analyses using mostly aposematic taxa supported this conclusion and proposed a single tandem origin of toxicity and conspicuous warning coloration. By using expanded taxon and character sampling, we reexamined the phylogenetic correlation between the origins of toxicity and warning coloration. At least four or five independent origins of aposematism have occurred within poison frogs; by using simulations, we rejected hypotheses of one, two, or three origins of aposematism (P < 0.002). We also found that diet specialization is linked with the evolution of aposematism. Specialization on prey, such as ants and termites, may have evolved independently at least two times.

Population Decline of the Jambato Toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador

Abstract The Jambato Toad, Atelopus ignescens, is endemic to montane forests, inter-Andean valleys, and paramos in Ecuador. Although formerly abundant and widely distributed, the species has not been recorded in nature since 1988. To determine its population status, data from intensive surveys in 1999–2001 are compared with those from 1967 and 1981. Presence-absence data from several localities also are reported. Temperature and precipitation between 1891 and 1999 were analyzed to determine whether these correlate with population trends. Atelopus ignescens was abundant in 1967 at Paramo de Guamaní (47 individuals recorded in 120 pers/min) and in 1981 at Paramo del Antisana (up to 0.75 individuals/m2). In the 1999–2001 surveys, A. ignescens was absent despite considerably higher survey efforts. The presence-absence data at several localities also indicate a dramatic decline. Before 1988, A. ignescens was present during 64% of the visits to sites throughout its range. After 1988, A. ignescens was absent at all sites. The results strongly suggest that A. ignescens is extinct. Climatic data show that 1987, the year previous to the last record of A. ignescens, was particularly warm and dry. The reasons for the decline in pristine areas remain unclear, although the available information suggests that a combination of factors such as pathogens and unusual weather conditions may have played an important role.

Evolution of Dietary Specialization and Chemical Defense in Poison Frogs (Dendrobatidae): A Comparative Analysis

Defensive mechanisms, including noxious or toxic substances, are favored by predation‐driven natural selection. The acquisition of noxious/toxic substances can be either endogenous, in which the substances are produced by the organism, or exogenous, in which the substances are produced by another organism and are sequestered. Evidence indicates that the defensive skin alkaloids of Neotropical poison frogs (Dendrobatidae) have an exogenous source: a diet of ants and other small alkaloid‐containing arthropods, which we term the diet‐toxicity hypothesis. A critical prediction of the diet‐toxicity hypothesis is that independent origins of dietary specialization will be found to be correlated with independent origins of skin alkaloids. We tested this prediction in an integrated framework using comparative methods with new and published data on feeding ecology and chemical defense for 15 species of dendrobatids in five genera. We found a significant correlation between alkaloid profiles and degree of dietary specialization. This reveals a recurring association of dietary specialization and alkaloid sequestration in dendrobatids, which suggests parallel evolutionary trends in the origins of defensive mechanisms.

Global warming and amphibian losses; The proximate cause of frog declines? (Reply)

Alford et al. question the working model underlying our test for a link between global warming and amphibian disappearances, and Di Rosa et al. criticize our emphasis on a single proximate agent, the chytrid fungus Batrachochytrium dendrobatidis. Both teams report key pieces of the amphibian-decline puzzle and new evidence from different parts of the world that climate change is a factor in these losses. Here we show why our working model was appropriate and highlight the complexity of the imminent threat to species survival that results as global warming conspires with various other agents.

A NEW, CRYPTIC SPECIES OF PHYSALAEMUS (ANURA: LEPTODACTYLIDAE) FROM WESTERN ECUADOR WITH COMMENTS ON THE CALL STRUCTURE OF THE P. PUSTULOSUS SPECIES GROUP

We describe a new species of leptodactylid frog of the genus Physalaemus from the lowlands of western Ecuador. It belongs to the P. pustulosus species group and differs from other group members in its smaller size, skin texture, tadpole characters, and advertisement call. The new species has wide variation in size and color pattern both at the intra- and inter-population levels. This variation matches that observed in P. montubio and P. randi, and render difficult its diagnosis on the basis of morphological features. A phylogenetic analysis of morphological characters shows that the new species belongs to a clade distributed west of the Andes in Ecuador and northern Peru, sister to (P. petersi + P. pustulosus). A phylogeny based on mtDNA shows that P. montubio and P. randi form a clade sister to (P. coloradorum + P. sp. nov.). The calls of these three species have two components with different acoustic features that arguably match the frequency sensitivity of the ear of conspecific females, in a manner similar to the complex calls of P. pustulosus. The new species occurs in two predominantly dry regions, the Lowland Deciduous Costa Forest, and the Lowland Semideciduous Costa Forest.

TWO NEW SPECIES OF ATELOPUS (ANURA: BUFONIDAE) FROM ECUADOR

Two new species of Atelopus from Ecuador are described; both are from the highlands of the Cordillera Occidental of the Andes, one from the Chimbo Basin and the other from the Páramos del Cajas. I include osteological data of both species and the description of the gastromyzophorous tadpoles of one of the new species. Patterns of diversity and endemism of Atelopus justify the necessity of further research and conservation efforts directed toward Andean habitats. Resumen Se reconocen dos especies de Atelopus de Ecuador nuevas para la ciencia; la una de la Hoya de Chimbo, la otra de los Páramos del Cajas; ambas provienen de regiones altas en la Cordillera Occidental de los Andes. Se proveen descripciones osteológicas de ambas especies y del renacuajo de torrente de una de las especies nuevas. Los patrones de diversidad y endemismo de Atelopus justifican la necesidad de mayores investigaciones biológicas y esfuerzos de conservación dirigidos a habitats andinos.

Assessing the molecular phylogeny of a near extinct group of vertebrates: the Neotropical harlequin frogs (Bufonidae; Atelopus)

Neotropical harlequin frogs, Atelopus, are a species-rich bufonid group. Atelopus monophyly has been suggested but intergeneric, interspecific and intraspecific relationships are poorly understood. One reason is that morphological characters of harlequin frogs are often difficult to interpret, making species delimitations difficult. Molecular analyses (DNA barcoding, phylogeny) may be helpful but sampling is hampered as most of the more than 100 Atelopus species have undergone severe population declines and many are possibly extinct. We processed mitochondrial DNA (12S and 16S rRNA) of 28 available ingroup samples from a large portion of the genus’ geographic range (Bayesian Inference, Maximum Likelihood). Our samples constitute a monophyletic unit, which is sister to other bufonid genera studied including the Andean genus Osornophryne. In contrast to previous morphological studies, our results suggest that Osornophryne is neither sister to Atelopus nor nested within it. Within Atelopus, we note two major clades with well supported subclades, one Amazonian–Guianan Clade (Flavescens-spumarius Clade plus Tricolor Clade) and an Andean–Chocó–Central American Clade (Varius Clade plus all other Atelopus). The first mentioned includes all species that possess a middle ear (i.e. stapes) except for A. seminiferus lacking it (like all remaining Atelopus). Previously proposed species groups based on frog-like versus toad-like overall appearance (i.e. Longirostris and Ignescens Groups) or phalangeal reduction in the thumb (i.e. Flavescens Group) are not monophyletic in our phylogeny, thus characters used to define them are not considered synapomorphies. We show that genetic divergence can be high between species belonging to different clades, in spite of their phenetic similarity (e.g. A. pulcher, Atelopus sp. 2). On the other hand, within the same clade, colour can vary tremendously, while genetic divergence is low (e.g. A. flavescens and allies). These observations demonstrate that Atelopus taxonomy is complicated and that an integrative approach is required before ‘splitting’ or ‘lumping’ nominal species.

Aposematism increases acoustic diversification and speciation in poison frogs

Multimodal signals facilitate communication with conspecifics during courtship, but they can also alert eavesdropper predators. Hence, signallers face two pressures: enticing partners to mate and avoiding detection by enemies. Undefended organisms with limited escape abilities are expected to minimize predator recognition over mate attraction by limiting or modifying their signalling. Alternatively, organisms with anti-predator mechanisms such as aposematism (i.e. unprofitability signalled by warning cues) might elaborate mating signals as a consequence of reduced predation. We hypothesize that calls diversified in association with aposematism. To test this, we assembled a large acoustic signal database for a diurnal lineage of aposematic and cryptic/non-defended taxa, the poison frogs. First, we showed that aposematic and non-aposematic species share similar extinction rates, and aposematic lineages diversify more and rarely revert to the non-aposematic phenotype. We then characterized mating calls based on morphological (spectral), behavioural/physiological (temporal) and environmental traits. Of these, only spectral and temporal features were associated with aposematism. We propose that with the evolution of anti-predator defences, reduced predation facilitated the diversification of vocal signals, which then became elaborated or showy via sexual selection.