Santiago R. Ron

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.

INTEGRATING PHYLOGENETICS AND ENVIRONMENTAL NICHE MODELS TO EXPLORE SPECIATION MECHANISMS IN DENDROBATID FROGS

Abstract We developed an approach that combines distribution data, environmental geographic information system layers, environmental niche models, and phylogenetic information to investigate speciation processes. We used Ecuadorian frogs of the family Dendrobatidae to illustrate our methodology. For dendrobatids there are several cases for which there is significant environmental divergence for allopatric and parapatric lineages. The consistent pattern that many related taxa or nodes exist in distinct environmental space reinforces Lynch and Duellmans hypothesis that differential selection likely played an important role in species differentiation of frogs in the Andes. There is also some evidence that the Río Esmeraldas basin is a geographic barrier to species distributed in low to middle elevations on the western side of the Andes. Another useful aspect of this approach is that it can point to common environmental parameters that correlate with speciation. For dendrobatids, sister clades generally segregate along temperature/elevational and/or seasonality axes. The joint analysis of environmental and geographic data for this group of dendrobatid frogs has identified potentially important speciation mechanisms and specific sister lineages that warrant intensive study to test hypotheses generated in this investigation. Further, the method outlined in this paper will be increasingly useful as knowledge of distribution and phylogeny of tropical species increases.

High levels of cryptic species diversity uncovered in Amazonian frogs

One of the greatest challenges for biodiversity conservation is the poor understanding of species diversity. Molecular methods have dramatically improved our ability to uncover cryptic species, but the magnitude of cryptic diversity remains unknown, particularly in diverse tropical regions such as the Amazon Basin. Uncovering cryptic diversity in amphibians is particularly pressing because amphibians are going extinct globally at an alarming rate. Here, we use an integrative analysis of two independent Amazonian frog clades, Engystomops toadlets and Hypsiboas treefrogs, to test whether species richness is underestimated and, if so, by how much. We sampled intensively in six countries with a focus in Ecuador (Engystomops: 252 individuals from 36 localities; Hypsiboas: 208 individuals from 65 localities) and combined mitochondrial DNA, nuclear DNA, morphological, and bioacoustic data to detect cryptic species. We found that in both clades, species richness was severely underestimated, with more undescribed species than described species. In Engystomops, the two currently recognized species are actually five to seven species (a 150–250% increase in species richness); in Hypsiboas, two recognized species represent six to nine species (a 200–350% increase). Our results suggest that Amazonian frog biodiversity is much more severely underestimated than previously thought.

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.

ANCIENT TEPUI SUMMITS HARBOR YOUNG RATHER THAN OLD LINEAGES OF ENDEMIC FROGS

The flattop mountains (tepuis) of South America are ancient remnants of the Precambrian Guiana Shield plateau. The tepui summits, isolated by their surrounding cliffs that can be up to 1000 m tall, are thought of as “islands in the sky,” harboring relict flora and fauna that underwent vicariant speciation due to plateau fragmentation. High endemicity atop tepui summits support the idea of an ancient “Lost World” biota. However, recent work suggests that dispersal between lowlands and summits has occurred long after tepui formation indicating that tepui summits may not be as isolated from the lowlands as researchers have long suggested. Neither view of the origin of the tepui biota (i.e., ancient vicariance vs. recent dispersal) has strong empirical support owing to a lack of studies. We test diversification hypotheses of the Guiana Shield highlands by estimating divergence times of an endemic group of treefrogs, Tepuihyla. We find that diversification of this group does not support an ancient origin for this taxon; instead, divergence times among the highland species are 2–5 Ma. Our data indicate that most highland speciation occurred during the Pliocene. Thus, this unparalleled landscape known as “The Lost World” is inhabited, in part, not by Early Tertiary relicts but neoendemics.

A NEW SPECIES OF FROG OF THE ELEUTHERODACTYLUS LACRIMOSUS ASSEMBLAGE (LEPTODACTYLIDAE) FROM THE WESTERN AMAZON BASIN, WITH COMMENTS ON THE UTILITY OF CANOPY SURVEYS IN LOWLAND RAINFOREST

We describe a new species of Eleutherodactylus from the lowlands of the western Amazon Basin. The new species is referred to the Eleutherodactylus unistrigatus group, lacrimosus assemblage. It differs from other members of the group by having a dorsal olive-green coloration with an interorbital creamy yellow stripe that extends posterolaterally and reaches the level of the sacrum, and low ulnar and tarsal tubercles. The new species inhabits western Amazon tropical rainforests and has been found in arboreal bromeliads by day and on vegetation by night. We discuss the effect of lack of sampling in the forest canopy in our understanding of tropical amphibian communities. Based on work conducted at two localities in Ecuadorian Amazonia, we find that even limited sampling effort in the canopy can greatly improve efficiency of biological inventories.

The evolution of female mate choice for complex calls in tungara frogs

Female mate preferences can favour the evolution of complex secondary sex traits in males. A mechanism increasingly explored to explain the origin of such male traits is sensory exploitation. Under sensory exploitation, female mating preferences are by-products of sensory biases that originate previously (often in nonreproductive contexts). Tungara frogs (Engystomops) have offered a widely known example for this mechanism. Male E. pustulosus make a complex call by adding a chuck to their typical whine call. Previous studies reported that the evolution of complex calls was driven by a female sensory bias that originated in the common ancestor of Engystomops, before the origin of complex calls. Here, I carry out mate choice experiments and new phylogenetic and comparative analyses to reevaluate the evolution of female mate choice and courtship calls in tungara frogs. My results indicate that the chuck and its corresponding female preference have coevolved in a process that is compatible with Fisherian or good genes sexual selection. Character reconstructions show that both the chuck and the female preference have originated multiple times among closely related lineages. I found no support for previously proposed scenarios of sensory exploitation in Engystomops, and the mate choice experiments indicated that increased stimulation of the sensory system by the male courtship signal does not necessarily translate into increased female preference. This finding highlights the significance of central processing in mate choice decisions.

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.

Human Influence on the Wariness of Melanosuchus niger and Caiman crocodilus in Cuyabeno, Ecuador

The effect of mark-recapture experiments on the wariness of Caiman crocodilus and Mela- nosuchus niger in two lakes in Amazonian Ecuador was examined. Three experiments were conducted with five, seven, and 10 sampling replicates, respectively. Each sampling replicate consisted of one nocturnal spotlight count around the lake, during which caimans were captured, marked, and released. There were negative correlations between the number of individuals seen in each sampling replicate and sampling replicate sequence in both lakes and both species. In one lake, there was a positive correlation between the percentage of wary caimans and the sequence of sampling replicates. Our findings indicate that observation and capture, even if harmless, affect the spatial distribution and wariness of crocodilian populations.

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.