Edgar Lehr

Batrachochytrium dendrobatidis and the Collapse of Anuran Species Richness and Abundance in the Upper Manu National Park, Southeastern Peru

Amphibians are declining worldwide, but these declines have been particularly dramatic in tropical mountains, where high endemism and vulnerability to an introduced fungal pathogen, Batrachochytrium dendrobatidis (Bd), is associated with amphibian extinctions. We surveyed frogs in the Peruvian Andes in montane forests along a steep elevational gradient (1200-3700 m). We used visual encounter surveys to sample stream-dwelling and arboreal species and leaf-litter plots to sample terrestrial-breeding species. We compared species richness and abundance among the wet seasons of 1999, 2008, and 2009. Despite similar sampling effort among years, the number of species (46 in 1999) declined by 47% between 1999 and 2008 and by 38% between 1999 and 2009. When we combined the number of species we found in 2008 and 2009, the decline from 1999 was 36%. Declines of stream-dwelling and arboreal species (a reduction in species richness of 55%) were much greater than declines of terrestrial-breeding species (reduction of 20% in 2008 and 24% in 2009). Similarly, abundances of stream-dwelling and arboreal frogs were lower in the combined 2008-2009 period than in 1999, whereas densities of frogs in leaf-litter plots did not differ among survey years. These declines may be associated with the infection of frogs with Bd. B. dendrobatidis prevalence correlated significantly with the proportion of species that were absent from the 2008 and 2009 surveys along the elevational gradient. Our results suggest Bd may have arrived at the site between 1999 and 2007, which is consistent with the hypothesis that this pathogen is spreading in epidemic waves along the Andean cordilleras. Our results also indicate a rapid decline of frog species richness and abundance in our study area, a national park that contains many endemic amphibian species and is high in amphibian species richness.

Thermal Physiology, Disease, and Amphibian Declines on the Eastern Slopes of the Andes

Rising temperatures, a widespread consequence of climate change, have been implicated in enigmatic amphibian declines from habitats with little apparent human impact. The pathogenic fungus Batrachochytrium dendrobatidis (Bd), now widespread in Neotropical mountains, may act in synergy with climate change causing collapse in thermally stressed hosts. We measured the thermal tolerance of frogs along a wide elevational gradient in the Tropical Andes, where frog populations have collapsed. We used the difference between critical thermal maximum and the temperature a frog experiences in nature as a measure of tolerance to high temperatures. Temperature tolerance increased as elevation increased, suggesting that frogs at higher elevations may be less sensitive to rising temperatures. We tested the alternative pathogen optimal growth hypothesis that prevalence of the pathogen should decrease as temperatures fall outside the optimal range of pathogen growth. Our infection-prevalence data supported the pathogen optimal growth hypothesis because we found that prevalence of Bd increased when host temperatures matched its optimal growth range. These findings suggest that rising temperatures may not be the driver of amphibian declines in the eastern slopes of the Andes. Zoonotic outbreaks of Bd are the most parsimonious hypothesis to explain the collapse of montane amphibian faunas; but our results also reveal that lowland tropical amphibians, despite being shielded from Bd by higher temperatures, are vulnerable to climate-warming stress.

Current State of Conservation Knowledge on Threatened Amphibian Species in Peru

This study documents the current state of conservation knowledge on threatened amphibian species in Peru. Following the International Union for the Conservation of Nature (IUCN) classification system, we considered species in the following categories: Critically Endangered, Endangered, Vulnerable, and Near Threatened. Even though only the first three categories are regarded as threatened by IUCN, we included the fourth category to make comparisons with the list of threatened species issued by the Peruvian government. We used the Global Amphibian Assessments database and the list issued in Peru for this comparison. We conducted separate field surveys in 17 regions of Peru to evaluate the presence/absence of threatened amphibian species and species that are potentially threatened. We also used the Declining Amphibian Database-DAPTF, to compare our results with previous assessments on population declines, and the World Wildlife Funds Wildfinder database, to determine in which Neotropical ecoregion each species occurs. We compiled data on 83 species, 44 of which are recognized as threatened by the IUCN and/or the Peruvian government. The remaining 39 species should be re-assessed as they face various threats. A re-evaluation of current estimates is needed as only 8% of all species recorded in Peru are recognized as threatened by the government, whereas the global estimate of threatened species is about 32%. In addition to using IUCN criteria, this re-assessment should follow national guidelines standardized in Peru and be in accordance with the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Because the habitat of almost 40% of threatened species reported herein still remains unprotected, and data on chytridiomycosis and other threats are lacking for most taxa, it is crucial to develop strategies for habitat conservation and research on disease dynamics in natural populations.

New Species of Bufo (Anura: Bufonidae) from Central Peru

Abstract A new species of toad, Bufo chavin, is described from two localities (3010 and 3070 m) from the eastern Andean slopes of central Peru (Departamento de Huánuco, Provincia de Pachitéa, Distrito de Chaglla) where it occurs sympatrically with Bufo spinulosus. Bufo chavin is referred to the Bufo veraguensis group. The new species differs from all members of this group by having large, elevated, elongate glands on each forearm and tibia, two large, elevated, elongate glands on the outer dorsal margin of each foot and one small, elevated gland on the outer dorsal margin of each hand. Eggs are relatively large, yolky and unpigmented in the new species. Se describe una nueva especie de sapo, Bufo chavin, procedente de dos localidades (3010 y 3070 m) en la vertiente oriental de los Andes del Perú central (Departamento de Huánuco, Provincia de Pachitéa, Distrito de Chaglla) donde se presenta simpátricamente con Bufo spinulosus. Bufo chavin es incluido al grupo Bufo veraguensis. La especie nueva difiere de todos los miembros de este grupo por tener una glándula larga, elevada y elongada en cada antebrazo y tibia; dos glándulas grandes, elevadas y elongadas en el margen dorsal externo de cada pie; y una glándula pequeña elevada en el margen dorsal externo de cada mano. En la especie nueva, los huevos son relativamente grandes, presentan abundante yema y no están pigmentados.

A Revision of Species Diversity in the Neotropical Genus Oreobates (Anura: Strabomantidae), with the Description of Three New Species from the Amazonian Slopes of the Andes

ABSTRACT We revisit species diversity within Oreobates (Anura: Strabomantidae) by combining molecular phylogenetic analyses of the 16S rRNA amphibian barcode fragment with the study of the external morphology of living and preserved specimens. Molecular and morphological evidence support the existence of 23 species within Oreobates, and three additional candidate species (Oreobates sp. [Ca JF809995], Oreobates sp. [Ca EU368903], Oreobates cruralis [Ca EU192295]). We describe and name three new species from the Andean humid montane forests of Departamento Cusco, southern Peru: O. amarakaeri New Species from Río Nusinuscato and Río Mabe, at elevations ranging from 670 to 1000 m in the Andean foothills; O. machiguenga, new species, from Río Kimbiri (1350 m), a small tributary of the Apurimac River, in the western versant of Cordillera Vilcabamba; and O. gemcare, new species, from the Kosñipata Valley at elevations ranging from 2400 to 2800 m. The three new species are readily distinguished from all other Oreobates by at least one qualitative morphological character. Three species are transferred to Oreobates from three genera of Strabomantidae: Hypodactylus lundbergi Pristimantis crepitans, and Phrynopus ayacucho (for which the advertisement call, coloration in life, and male characteristics are described for first time). Oreobates simmonsi is transferred to the genus Lynchius. Hylodes verrucosus is considered a junior synonym of Hylodes philippi. In addition, H. philippi is removed from the synonymy of O. quixensis and considered a nomem dubium within Hypodactylus. The inclusion of Phrynopus ayacucho in Oreobates extends the ecological range of the genus to the cold Andean puna. Oreobates is thus distributed from the Amazonian lowlands in southern Colombia to northern Argentina, reaching the Brazilian Atlantic dry forests in eastern Brazil, across an altitudinal range from ca. 100 to 3850 m.

A New Species of Minute Noblella (Anura: Strabomantidae) from Southern Peru: The Smallest Frog of the Andes

Abstract We describe a new species of Noblella from the upper Cosñipata Valley in southern Peru (Cusco Region). Specimens were found in the leaf litter of a cloud forest between 3025 and 3190 m elevation. The most distinctive character of the new species is its diminutive size (maximum SVL female 12.4 mm, male 11.1 mm). With an average snout–vent length of 11.4 mm (n  =  7) in adult specimens, the new species is the smallest Andean frog, and one of the smallest anurans in the world. The new frog is rare (between 30 and 75 frogs/ ha) and found only in montane scrub and forest habitats near the ecotone with the high-Andean puna grasslands. Although the amphibian fungal infection (Batrachochytrium dendrobatidis) has been recorded in southern Peru, no infections were detected in the new species.

Analysis of Andes Frogs (Phrynopus, Leptodactylidae, Anura) Phylogeny Based on 12S and 16S Mitochondrial rDNA Sequences

South American leptodactylid frogs of the genus Phrynopus occur in cloud‐forest, páramo, subpáramo and puna habitats (1000–4400 m elevation) from Colombia to Bolivia. Currently, there are 34 described species; however, many additional species new to science have been reported from Colombia, Peru, and Bolivia. The phylogeny of the species‐diverse Phrynopus is unknown and the position of the genus within Leptodactylidae is poorly understood. We present the results of a phylogenetic study based on 12S and 16S mitochondrial rDNA. Fifteen species of Phrynopus from Bolivia to Ecuador are included, along with several other genera of Leptodactylidae and representatives of other frog families. Our results indicate that Phrynopus is phylogenetically nested within Eleutherodactylus, whereas Phyllonastes is phylogenetically nested within Phrynopus. Based on the recovered phylogeny, we transfer Phrynopus simonsii to Eleutherodactylus, and show that Phrynopus carpish needs to be removed from Phrynopus. Eleven of the 13 Phrynopus species occurring in Central Peru share the absence of an external and internal ear.

A STRIKING NEW SPECIES OF ELEUTHERODACTYLUS FROM ANDEAN PERU (ANURA: LEPTODACTYLIDAE)

A new species of the Eleutherodactylus unistrigatus group is described from forests near Oxapampa, Peru, at elevations of 2050–2200 m in the Cordillera Oriental in central Peru. The new species differs from all described species by having an extremely long, acuminate snout and a red (white in preservative) longitudinal stripe on the posterior surface of each thigh.

The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru

We compile a list of all amphibians and reptiles known to occur within Manu National Park, Peru and its buffer zone, located in one of the worlds biodiversity hotspots. Covering approximately 0.01% of the planets terrestrial surface, this protected area preserves 155 species of amphibians and 132 species of reptiles, corresponding to 2.2% and 1.5% respectively of the known diversity for these groups. Moreover, Manu National Park preserves natural habitats and populations of one critically endangered (Atelopus erythropus), three endangered (Bryophryne cophites, Pristimantis cosnipatae and Psychrophrynella usurpator), three vulnerable amphibians (Atelopus tricolor, Gastrotheca excubitor, Rhinella manu) and two vulnerable reptiles (Chelonoidis denticulata, Podocnemis unifilis), according to the threat categories of the IUCN Red List.

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.