Research Article |
Corresponding author: Juan Pablo Reyes-Puig ( juanpabloecominga@gmail.com ) Academic editor: Luis Ceríaco
© 2022 Juan Pablo Reyes-Puig, Carolina Reyes-Puig, Daniela Franco-Mena, Lou Jost, Mario H. Yánez-Muñoz.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Reyes-Puig JP, Reyes-Puig C, Franco-Mena D, Jost L, Yánez-Muñoz MH (2022) Strong differentiation between amphibian communities on two adjacent mountains in the Upper Rio Pastaza watershed of Ecuador, with descriptions of two new species of terrestrial frogs. ZooKeys 1081: 35-87. https://doi.org/10.3897/zookeys.1081.71488
|
We present the results of herpetological surveys in two adjacent mountains where the EcoMinga Foundation protects the cloud forest in the Upper Rio Pastaza watershed, in the Llanganates Sangay Ecological Corridor in Ecuador. A rapid assessment of the amphibian communities of the study sites reveals a diverse and heterogeneous composition, dominated by terrestrial frogs from the genus Pristimantis. We also identify a cryptic diversity with a significant number of candidate new species. We describe two new species of terrestrial frogs of the genus Pristimantis. Pristimantis maryanneae sp. nov. is characterised by not having tympanum externally visible and having 2–3 subconical tubercles in the upper eyelid; and Pristimantis burtoniorum sp. nov. is characterised by the presence of red colouration in hidden surfaces of the hind-limbs, tubercles on the upper eyelid, interorbital tubercle and a row of rounded tubercles along the snout to the tip and a pale red venter with dark brown mottled pattern. Our samples from the two Reserves do not share species between them, so the proportion of shared species seems to be relatively low. In addition, we highlight the importance of updating the knowledge of amphibians that are restricted to this important conservation region and comment about the threats and composition of the amphibian communities on the eastern slopes of the Upper Rio Pastaza watershed.
Andes, conservation, endemism, Llanganates-Sangay Ecologic Corridor, montane cloud forest, Pristimantis
Ecological systems extending along the Cordillera Oriental of the Ecuadorian Andes harbour great amphibian diversity, with many locally-endemic species (Duellman 1978;
The ecological corridor between Llanganates and Sangay National Parks in the Upper Rio Pastaza watershed of Tungurahua and Pastaza Provinces in east-central Ecuador was declared a “Gift to the Earth” by the World Wildlife Fund in 2002, due to the great biodiversity and endemism that it houses in a small geographical area (
The Llanganates National Park and its surroundings remain one of the least explored regions nationwide (
We sampled the Machay Reserve and Naturetrek-Vizcaya Reserve (Table
Amphibian sampling and description of sites: Machay Reserve and Naturetrek-Vizcaya Reserve, Tungurahua Province.
Reserve | Point | Coordinates Elevation (m) | Description | Collection sources | Sampling units | Sampling effort | Days sampled | Hours per person |
---|---|---|---|---|---|---|---|---|
Naturetre-Vizcaya Reserve (NR) | NVR1 | -1.358593, -78.394711; 2300 m elev. | Montane cloud forest along a mountain ridge; trees between 15 to 20 m tall with a small number of epiphytes; soil with much leaf litter, dense undergrowth and rocky outcrops. | Transects: 1000 X 2 m / 5 hours*3 persons | 1 | 2000 m / 15 hours/person | 3 | 15 |
Pitfall 75 m | 7 | 75 m | 7 | - | ||||
Naturetre-Vizcaya Reserve (NR) | NVR2 | -1.356007, -78.388436; 2730 m elev. | Evergreen montane forest along a mountain ridge, trees from 20 to 25 m tall, of “Cedar” (Cedrella), Myrtle (Myrcianthes), Chigmay (Ilex sp.), Tarqui (Hedyosmum) and wax palm (Ceroxylum). Undergrowth dominated by Poaceae, abundant bryophytes and epiphytes. | Transects: 1000 X 2 m / 5 hours*3 persons | 1 | 2000 m / 15 hours/person | 3 | 15 |
Pitfall 75 m | 7 | 75 m | 7 | - | ||||
Naturetre-Vizcaya Reserve (NR) | NVR3 | -1.360379, -78.399926; 2180 m | Riparian montane cloud forest with trees 20 m tall, such as I, Cedrella, Zapoteca aculeate, several palms and Ishnosiphon shrubs | Transects: 500 X 2 m / 5 hours*3 persons | 1 | 1000 m / 15 hours/person | 3 | 15 |
Machay Reserve (MR) | MER1 | -1.395952, -78.272943; 2200 m elev. | Primary mountain mist forest on a mountain ridge with trees of 20 to 25 m tall, abundant bryophytes and epiphytes covering the trees, mainly Magnolia (Magnoliaceae), Myrtle (Myrcianthes), Lauraceae and different palms. | Transects: 1000 X 2 m / 5 hours*3 persons | 1 | 2000 m / 15 hours/person | 3 | 15 |
Machay Reserve (MR) | MER2 | -1.387766, -78.266388; 2450 m elev. | Evergreen montane forest, with abundant epiphytes. The forest is relatively low between 15 to 20 m tall, including Pumamaqui (Oreopanax sp.), Clusea, and others. The undergrowth is dominated by Espadaña (Neurolepis sp.). | Transects: 1000 X 2 m / 5 hours*3 persons | 1 | 2000 m / 15 hours/person | 3 | 15 |
Machay Reserve (MR) | MER3 | -1.366561, -78.270336; 3030 m elev. | Tall montane evergreen forest, with trees ranging from 15 to 20 m tall; the soil and trees are completely covered by a thick layer of bryophytes and epiphytes, especially a large number of bromeliads, Clusea and Podocarpus trees. | Transects: 1000 X 2 m / 5 hours*3 persons | 1 | 2000 m / 15 hours/person | 3 | 15 |
The Naturetrek-Vizcaya Reserve (NVR) is located within the Ulba Parish, bordering the Llanganates National Park. This Reserve was initiated in 2012 with support from the Naturetrek via the World Land Trust and new forest blocks have been added during the last few years, forming approximately 150 hectares of montane cloud forest between 2200 and 3000 m above sea level. The sample points, evaluated during our expeditions, are presented in Table
These two main sites are compared to four other EcoMinga Reserves in the Llanganates-Sangay Ecological Corridor: the Rio Anzu Reserve, Rio Zuñag Reserve, w – Cerro Candelaria Reserves and Chamana Reserve (Figs
Sample points in the Naturetrek-Vizcaya Reserve (black triangles) and the Machay Reserve (black circles). The white triangle is the type locality of Pristimantis maryanneae sp. nov. and the white circle is the type locality of Pristimantis burtoniorum sp. nov. The grey shaded areas are the Reserves of the EcoMinga Foundation within the Llanganates-Sangay Corridor and the green shaded areas represent Llanganates National Park (north) and Sangay National Park (south).
During February and March 2018, we carried out herpetological surveys in six sampling areas (Table
The standardised techniques used for sampling amphibians, with their respective sampling efforts, are summarised in Table
Visual Encounter Surveys (VES) (
Transects of Auditory Bands (TBA) (Rueda et al. 2006): this technique is based on the vocalisations emitted by adult males, which are specific to each species. This method consists of counting males singing along a transect with a predetermined length (i.e. 1000 m), whose width varies according to the detection distance of the song of the focal species; that is, the maximum distance at which the animal can be heard by the observer. Individuals encountered were observed and captured and vocalising males were recorded using previously established protocols. In the case of vocalising males, the number of calls per species was recorded along intervals of the sampling unit in their respective sample area.
Pitfall traps (Voss et al. 1996; Rueda et al. 2016): due to the topography and accessibility of the terrain, we established in the NVR three linear transects of 75 m with 10 buckets of 20 l capacity, once every 7 m, to sample terrestrial leaf litter frogs. Buckets were checked every morning for twenty days.
Photographic records. We used EcoMinga reserve rangers photographs of individuals found in opportunistic sampling taken from MR. After a detailed revision of images, we registered individuals whose taxonomic identity could be confirmed from the photos.
Each specimen captured was assigned a unique record number and the specimen was taken to the base camp in an individual plastic bag to confirm its sex or relative age. We recorded time of capture, type of vegetation in which it was captured, substrate, activity, and climatic conditions. To facilitate the identification of dorsal, ventral and flank patterns, each specimen was photographed with a unique code number and stored in a catalogue of photographic references.
To physically and permanently document the identification of the specimens, we deposited series of voucher specimens (Foster 2002) at the División de Herpetología (DHMECN) of the Instituto Nacional de Biodiversidad (INABIO), located in Quito, Ecuador. The specimens were fixed in formalin at 10% concentration and definitively preserved in 70% alcohol (
The description of the species follows
We generated descriptive statistics from a general double-entry diversity matrix; we tabulated the data produced in two sampling sites and then abundance-diversity figures were applied for each of the sites analysed. The data were initially tabulated and then the analyses available in the BioDiversityPro ver.2 package were applied (
The standardised samples, obtained from the transects, were further analysed to compare the diversities of the Machay and Naturetrek-Vizcaya Reserves. Two types of rarefaction were applied, to correct for between-reserve differences in number of individuals, sampling effort and sample completeness (
An exploratory post-hoc linear regression of log10 SVL versus elevation was conducted on the eighteen adult females from the genus Pristimantis (the more abundant genus) of both sites, regardless of species. This analysis was not intended to test a previously-established hypothesis, since it was carried out later; however, we wanted to inspect the general pattern and describe it for future studies related to the variation in body size.
The species recorded were classified according to distribution, threat level and reproductive strategies using the following categories:
Distribution Range: IN = Introduced, NE = Not Evaluated, WN = Wide Neotropical distribution, EC = Endemic of Ecuador, AN = Endemic from the Andes.
Extinction Risk IUCN (2019): NE = Not Evaluated, LC = Least Concern, NT = Near Threatened, VU = Vulnerable, EN = Endangered and CR = Critically Endangered.
Reproductive strategies
: We use the classification system of reproductive modes or strategies of
During surveys, we recorded 97 individuals of anurans grouped into seven genera and five families (Fig.
In the Machay Reserve, 78 individuals were registered; the community was composed of 17 species, led by terrestrial frogs (Fig.
In the Natutretrek Viscaya Reserve, 19 individuals were registered, including captured and calling individuals; the community was composed of six species. The number of individuals registered comprise 22% of the total number of individuals recorded for the two Reserves. The dominant species was the rain frog Pristimantis tungurahua, followed by Pristimantis maryanneae and Noblella naturetrekii; the remaining species had abundances between one and two individuals (Fig.
A Conservation status categories of the amphibian composition from the Machay Reserve and the Naturetrek-Vizcaya Reserve, under the IUCN Red List and ARLE Amphibian Red List Ecuador (
80% of the recorded species do not have a regional or global conservation status. Many of these taxa are not formally described; thus, categorising their range distribution is work that must be done in the future. The remaining 20% of the species correspond to Vulnerable, Endangered and Critically Endangered species. Nonetheless, some taxa are species complexes and need their taxonomical relationships clarified. On the other hand, all of the species with a taxonomic identity (i.e. formally described) are restricted to the eastern Andean slopes and 55.5% of these species are completely restricted to the upper Rio Pastaza watershed within Tungurahua Province (Fig.
We found that log10 SVL (in mm) of individual adult females (all given equal weight, without regard to species) showed a weak negative correlation with elevation (in metres). The least squares line (with 95% confidence intervals) had a slope of -0.00022 (-0.00002 to -0.0004) and an intercept (extrapolated log10 SVL at sea level) of 1.9 (1.36 to 2.37); r2 = 0.3 and p = 0.03. We give this p-value only for reference; since this was a post hoc analysis, p-values do not have a simple interpretation. The fitted line predicts a SVL of 27.5 mm (21 mm to 36 mm) at 2000 m elevation and a SVL of 17 mm (13 mm to 21 mm) at 3000 m elevation (Fig.
Five breeding modes (
Anuran reproductive strategies within Naturetrek-Vizcaya Reserve and Machay Reserve. Types of reproductive strategies I.-A Eggs hatch in exotropic tadpoles that are carried to lentic water. Eggs and feeding tadpoles in lentic water I.-B Eggs hatch in exotropic tadpoles that are taken to lotic waters. Eggs and feeding tadpoles in lotic water II.-A Eggs with direct development, completely formed hatched frogs II.-B Eggs imbedded in dorsum of aquatic female; eggs hatch into froglets III.-A Ovoviviparous; nutrition is provided by the yolk.
Our standardised transect sampling on the two mountains revealed both a higher density of individuals and higher number of species in the Machay Reserve. In the Machay Reserve, there was a density of 1.7 individuals per sampling hour per person, while in the Naturetrek-Vizcaya Reserve, the density was only about 1/4 of this, at 0.4 individuals per sampling hour per person. Twelve species were observed on transects in the Machay Reserve, while only four species were observed on transects in the Naturetrek-Vizcaya Reserve. The transect sample from the Machay Reserve has a completeness or sample coverage of 87%, while that of the Naturetrek-Vizcaya Reserve has a completeness or sample coverage of 83%. Sample coverage is the proportion of the community’s population that belongs to species detected by the sample (
To determine whether the higher diversity of the Machay Reserve was real or was merely due to the higher density of individuals encountered there, we examined the rarefaction curves for the two sites. The standard rarefaction or species accumulation curve for the Machay sample was always significantly above the curve for the Naturetrek-Vizcaya sample (Fig.
Interpolated and extrapolated species accumulation curves versus number of individuals for the Machay and Naturetrek-Vizcaya Reserves. The black vertical line marks the number of individuals at which the richness of each are compared on each curve (this is the size of the smallest sample). At this sample size (n =11), the sample from Naturetrek-Viscaya would on the average have three species, while a sample of the same size from Machay would be expected to have five species.
Interpolated and extrapolated species accumulation curves versus sample coverage (percent of the population represented by species in the sample) for the Machay and Naturetrek-Vizcaya Reserves. The black vertical line marks the number of individuals at which the richness of each are compared on each curve (this is the coverage of the least complete sample). At this coverage, the sample from Naturetrek-Viscaya would on the average have three species, while a sample of the same coverage from Machay would be expected to have six species.
The amphibian community at the six studied localities of the upper Rio Pastaza watershed was heterogeneous (Appendix
Comparison matrix of diversity data in six EcoMinga Reserves of the Upper Rio Pastaza watershed. In bold and white, number of species per site. Above the species line, in italics, percentage of shared species. Below the species line, linear distance in kilometres between sites compared.
Location | Sites | AR | ZR | MR | NVR | CR | NCCR | Unique species per site |
---|---|---|---|---|---|---|---|---|
Northern Pastaza | AR | 39 | 11 | 4 | 0 | 0 | 19 | 19 |
Northern Pastaza | ZR | 13 | 32 | 11 | 0 | 3 | 21 | 10 |
Northern Pastaza | MR | 24 | 11 | 18 | 0 | 8 | 4 | 11 |
Northern Pastaza | NVR | 39 | 25 | 14 | 6 | 15 | 4 | 2 |
Southern Pastaza | CR | 30 | 17 | 7 | 12 | 9 | 7 | 2 |
Southern Pastaza | NCCR | 35 | 22 | 11 | 7 | 5 | 36 | 10 |
Lower elevation limit in metres | 1050 | 1400 | 1500 | 2300 | 2300 | 1500 | – | |
Upper elevation limit in metres | 1300 | 2200 | 3030 | 2700 | 2700 | 3860 | – | |
Coordinates | -1.358593°, -78.394711° | -1.358593°, -78.394711° | -1.366561°, -78.270336° | -1.358593°, -78.394711° | -1.358593°, -78.394711° | -1.358593°, -78.394711° |
The number of species and number of individuals per family in each locality were highest in the Anzu Reserve and Naturetrek-Cerro Candelaria Reserves. Rain frogs (Strabomantidae) are the predominant family in all six Reserves. At a regional scale, tree frogs (Hylidae) have significantly reduced diversity, compared to the Terrarana (Strabomantidae) and the proportions of the remaining families, such as Bufonidae, Centrolenidae, Leptodactylidae, Hemiphractidae, and Dendrobatidae, are not constant in the Reserves of the Upper Rio Pastaza watershed (Fig.
The degree of similarity according to the Jaccard Index reflects that the composition amongst the six localities only shared 11% similarity, Zuñag and Anzu Reserves are more similar, sharing only 27% of their species and present high diversity of elements typical from lowland Amazonian tropical forest mixed with montane species. The cluster analysis defines highly heterogeneous communities between Reserves, showing different composition of anuran assemblages delimited by topography north and south to the Pastaza River and its proximity to the highland Andes or the Amazon Basin (Figs
We recorded three adult female specimens (DHMECN 14412-14413-14414) with body sizes between 26.58 mm and 33.57 mm collected at night on bromeliad leaves, palms and Neurolepis (Poaceae), between 40 cm and 170 cm from the ground and a juvenile (DHMECN 14415) with body size 12.38 mm, collected in a bromeliad 20 cm from the ground. According to the original species description, O. simpsoni was known only from two localities in the upper Rio Pastaza watershed and Cordillera Abitahua (Páez et al. 2012). The record in Machay Reserve corresponds to the third locality of the species within Ecuador. This taxon is characterised by having Toes IV and V longer than Toes I–III, a short and rounded snout with a small rostral papilla and conical pustules on flanks. This species of plump toad inhabits the high montane forests of the Machay Reserve, between 2430 and 2490 m in elevation, this forest being characterised by low trees with abundant bryophytes and bromeliads. Under direct manipulation, this species tends to escape with slow movements and lets itself fall in a ball-like position.
This species was recorded in riparian vegetation through previous observations in nearby localities, by auditory and a recent voucher specimen record (DHMECN 16217) in montane forests of the Naturetrek-Vizcaya Reserve from 2270 to 3000 m elevation. According to a photograph, the specimen may be associated with the C. buckleyi species group (
The marsupial frogs of the genus Gastrotheca were recorded by audio records, but were difficult to capture, in the cliffs and southern montane forests of the Naturetrek-Vizcaya Reserve at 2270 m elevation. The auditory records analysed are similar to those issued by Gastrotheca riobambae (Fowler, 1913) which has been recorded a few kilometres from Naturetrek-Vizacaya Reserve in the locality of El Triunfo (
We recorded a female specimen (DHMECN 14416) with a body size of 73.71 mm and a male (DHMECN 14549) with a body size of 54.28 mm, collected in bromeliad leaves between 40 and 60 cm from the ground, in montane forest of the Machay Reserve at 3020 m elevation. They correspond to a candidate new species of the genus Hyloscirtus in the H. larynopigion species group. The distinctive dark brown body with scattered bright red dorsal and ventral spots in the female (DHMECN 14416) and the irregular mustard-brown dorsal marks and black flanks in the male (DHMECN 14549), differentiate it from any other congeneric species in the eastern Andean slopes of Ecuador. The analysed material fills a gap in the distribution of the genus Hyloscirtus, specifically of the H. larynopigion species group, within the south-central area of the eastern Ecuadorian Andes. This finding represents the first record of a member of the Hyloscirtus larynopigion species group in Tungurahua Province. The species presents a marked sexual dimorphism between males and females as mentioned before. A formal description of this new species is currently under preparation.
These records correspond to a candidate new species; this is a new terrestrial frog very different from the Niceforonia elassodisca expected to be found in the region. Two female specimens (DHMECN 14417-14418) with body sizes of 16.36 mm to 16.95 mm, one male individual (DHMECN 14419) with body size of 19.15 mm and one immature specimen (DHMECN 14488) with body size of 12.73 mm, were collected between dry leaves of Clusia and bulrush in the leaf-litter in montane forest of the Machay Reserve between 2480 and 2960 m elevation. Its uniformly cream-coloured ventral pattern clearly distinguishes it from H. elassodisca. Niceforonia elassodisca has a dark venter and no defined subocular and supratimpanic cantal bands, while Niceforonia sp. has a defined subocular and supratimpanic cantal band, as well as a dark brown anal ornamentation.
A recently described species (Reyes-Puig et al. 2019), we recorded a male specimen (DHMECN 14437) with body size of 17.44 mm and a female specimen (DHMECN 14420) with body size of 14.92 mm, collected in the Naturetrek-Vizcaya Reserve at 2390 m elevation. These specimens correspond to the first records of the genus over 2000 m above sea level in the eastern Andean slopes of Ecuador. Both specimens were captured in pitfall traps. This species differs from its congeners by the presence of a differentiated tympanic membrane and a weakly-defined tympanic annulus, eyelids with rounded tubercles, blackish-dark brown ventral colouration scattered with little white dots and the absence of papillae at the tip of the fingers and toes, unlike Noblella colomai, N. personina, N. myermecoides, N. lochites and N. heyeri that have visible tympanic annuli and pale or colourful bellies.
We collected two female specimens (DHMECN 14423-14424) with body sizes of 21.33 mm up to 22.40 mm and two male specimens (DHMECN 14421-14422) with body sizes of 15.58 mm up to 16.73 mm; the specimens were found on bush, palm and cyclanth leaves between 20 cm and 50 cm from the ground in montane Machay Reserve forests at 2290 m elevation. This species is characterised by having a distinctive pattern of irregular white marks on the black venter, conical tubercles on the upper eyelid, one interorbital tubercle and a row of ulnar and tarsal tubercles.
This record extends the known distribution of the species, since the available records had been restricted to a few localities near the Tungurahua Volcano (
We recorded a female specimen (DHMECN 14426) with body size of 28.83 mm collected on a palm leaf in the montane forests of the Machay Reserve at 2290 m elevation. This specimen corresponds to the first record of P. tinguichaca on the north side of the Rio Pastaza and extends its altitudinal distribution in the Province of Tungurahua from the previous record of 2470 m (
We documented three female specimens (DHMECN 14427, 14428, 14429, 14433) with body sizes of 20.15 mm up to 22.87 mm, two male specimens (DHMECN 14430, 14431) with body sizes of 15.87 mm up to 16.77 mm and one juvenile specimen (DHMECN 14432) with a body size of 14.02 mm; the specimens were collected on leaves of ferns and shrubs between 30 cm and 40 cm from the ground and dry sticks between leaves at ground level; some of them were captured in pitfall traps. These specimens and others in the Chamana Reserve correspond to the first records since the original description (Reyes-Puig et al., in preparation); these records extend the limits of altitudinal distribution to the range of 2400 m to 2900 m. This species can be easily distinguished by its distinctive red salmon colouration on the groin, ventral surfaces of the limbs and by the presence of dorsolateral folds.
Two specimens (DHMECN 14434-14435) of body sizes between 21.64 mm and 27.97 mm were collected on a Clusia leaf 110 cm from the ground, in the montane forests of Cerro Mayordomo at 3000 m elevation. This is species is characterised by low dorsolateral folds and an areolate venter.
One female specimen (DHMECN 14436) with body size of 25.53 mm, a male specimen (DHMEN 14437) with body size of 11.37 mm and five male specimens (DHMECN 14438- 14439-14487-14440-14441) of body sizes of 15.3 mm up to 22.91 mm, were collected on bush leaves and branches 170 cm from the ground, in Machay Reserve montane forests at elevations ranging from 2230 m to 2310 m. This species had already been registered in other EcoMinga Reserves, such as the Cerro Candelaria Reserve and the Río Zuñag Reserve. This species is characterised by having a conical tubercle on the upper eyelid and the heel and by having coppery to red iris in females, dark yellow in males.
Five female specimens (DHMECN 14446, 14447, 14448, 14484, 14705) with body sizes of 13.58 mm up to 19.03 mm, three male specimens (DHMECN 14449-14450, 1486) with body sizes of 12.6 mm up to 15.02 mm and one specimen with undetermined sex (DHMECN14485) with a body size of 11.35 mm, were collected on the forest floor between the leaf litter and on a bromeliad leaf 30 cm from the ground, in the montane forests of the Machay Reserve at elevations between 2220 m to 3000 m. This species has been recorded in other localities, such as Cerro Candelaria Reserve, Chamana Reserve and Tungurahua Volcano; however, some preliminary phylogenetic analyses suggest that northern and southern forms correspond to distinct near-related species (Franco, in preparation). According to references and historical records, the specimens assigned to Pristimantis festae of the Tungurahua Volcano (
Two male specimens (DHMECN 14443-14706) with a body size of 15.77 to 19.43 mm and one female specimen (DHMECN 14707) with a body size of 19.71 mm were collected on bush leaves at 100 cm from the ground, in the montane forests of the Machay Reserve at 2430 m elevation. The external morphology and colouration pattern are somewhat similar to Pristimantis eriphus; however, the latter has red eyes and white spots in the groin, as opposed to the yellowish spots and coppery yellow iris of the present species.
A specimen (DHMECN 14444) of body size of 19.5 mm was collected on a dry branch 120 cm from the ground, in Machay Reserve montane forests at 2320 m elevation. This species is characterised by having small subconical tubercles on the upper eyelid and heel and brown dorsum.
A specimen (DHMECN 14445) of body size of 21.04 mm was collected on a fern leaf 110 cm from the ground, in the montane forests of Machay Reserve at 2600 m elevation. This species is very similar to Pristimantis tungurahua found in nearby localities, such as the Cerro Candelaria Reserve, Naturetrek-Vizcaya Reserve and Chamana Reserve. However, the Machay Reserve’s specimen differs in that it has patterns with white spots in the groin and ventral surfaces, as opposed to the red belly and dark colour of P. tungurahua.
We recorded a specimen (DHMECN 14455) of body size of 11.67 mm, collected on bush leaves in the montane forests of the Machay Reserve at 3030 m elevation. This species is characterised by having conical tubercles on all dorsal surfaces with green and brown tones on the body and also presenting a rostral papilla at the tip of the snout.
We recorded four specimens (DHMECN 14456-14457-14458-14459-14460-14461) with body sizes between 12.28 mm up to 16.85 mm, collected in the montane forests of the Machay Reserve at 3030 m elevation. This species is characterised by having subconical tubercles in the dorsal surfaces of the head and dorsum brown to copper with dark venter.
We recorded four specimens (DHMECN 14462-14463-14464-14465) of body sizes between 15.10 mm and 22.93 mm collected in bromeliads in the montane forests of Machay Reserve. This species is characterised by having conical tubercles on the upper eyelid, dorsolateral folds and a distinctive colouration pattern on the flanks, groin and hidden surfaces of the thigh characterised by a brown background with white spots.
We recorded two female specimens (DHMECN 14466-14703) with body sizes of 34.94 mm to 39.44 mm, four juvenile specimens (DHMECN 14472-14473-14474-14475) with body sizes of 14.29 mm to 16.25 mm and six male specimens (DHMECN 14467-14469-14468-14470-14471, 14704) with body sizes of 20.35 mm to 27.5 mm. The specimens were collected on leaves and branches of shrubs, bromeliads, ferns, and bulrush between 50 cm and 175 cm from the ground, in the montane forests of the Machay Reserve at elevations between 1990 to 3000 m above sea level. This species in its external morphology resembles the Pristimantis devillei group; however, Pristimantis sp. D exhibits tubercles on the upper eyelids and on the external edge of the tarsus.
A specimen (DHMECN 14476) with body size of 20.49 mm was collected on a bush leaf at 170 cm in the montane forests of MER at 2970 m elevation. Due to its external morphology, this species could be related to the Pristimantis lacrimosus group; however, all known species of that group are found only below 2000 m elevation. This species could be the highest record for the Pristimantis lacrimosus group.
Holotype. DHMECN 14454 (adult male Fig.
Paratypes (1 female, 3 males). DHMECN 14451 (♂ adult male), DHMECN 14453 (juvenile), with same location data as the holotype; DHMECN 14452 (♂ adult male) with same location data as the holotype, collected on 27 February 2018 and DHMECN 14550 (♀ adult female) with the same location data as the holotype, collected on 15 February 2018.
We assign the new species to Pristimantis, based on having head about as wide as body; cranial crests absent; dentigerous process of vomers present; “S” condition of the adductor muscles; terminal discs on digits, bearing well-defined circumferential grooves, supported by T-shaped terminal phalanges; Toe V as long as, or longer than, Toe III; and subarticular tubercles not protruding (Hedges 2008).
Pristimantis maryanneae can be distinguished from other Pristimantis by the following character combination: (1) skin on dorsum finely shagreen, with flat and low warts, weak and fine sacral fold, composed of some low warts, two pairs of scapular tubercles diagonal aligned behind the eye; venter areolate with pustules, discoidal fold present; (2) tympanum absent, hidden beneath the skin; tympanic anulus visible under the skin measuring 25% of the eye diameter; (3) snout short, rounded in dorsal and lateral profile; (4) upper eyelid with 2–3 subconical tubercles (rounded in preservative); upper eyelid wider than interorbital distance; cranial crests absent; (5) dentigerous process of vomer present, oblique in outline with 2–3 oval teeth; (6) males without vocal slits, no nuptial pads; (7) Finger I shorter than II; digital pads expanded; (8) fingers with weakly defined laterals fringes; (9) forearms with small ulnar subconical tubercles; (10) heel bearing a small subconical tubercle; outer edge of tarsus bearing small subconical tubercles, inner tarsal fold absent; (11) two metatarsal tubercles, inner oval twice or three times larger than outer oval that is subconical; (12) toes without lateral fringes; supernumerary tubercles present, Toe V larger than III, does not reach distal subarticular tubercle of Toe IV; (13) dorsal colouration dark grey to grey with green marks, with transverse dark brown marks, with a chevron and irregular “H” shaped marks, flanks with cream diagonal bands, shanks with cream diagonal bands and light brown interspaces, hind-limbs with grey transverse bands and dark brown interspaces; ventral colouration dirty cream with a line along middle of the venter, chin and outer mandibula mottled with dark brown marks, iris light brown to grey with black reticulation and horizontal coppery stripe and (14) SVL males 17.61–17.8 mm; female 21.06mm.
(Fig.
Live photograps of new species and comparison with similar Pristimantis frogs in the region A Pristimantis burtoniorum sp. nov. (DHMECN 16220 from Machay Reserve Cerro Mayordomo.) B P. maryanneae sp. nov. (DHMECN 14454 from Naturetrek Vizcaya Reserve) C P. prolatus (DHMECN 16244 from El Encanto) D P. albujai (DHMECN 12245 from Sardinayacu river) E P. tungurahua (DHMECN 15224 from Naturetrek Vizcaya Reserve) F P. puruscafeum (not collected from Cerro Candelaria Reserve) G P. sacharuna (DHMECN 16723 from Rio Zuñag Reserve) H P. ventrimarmoratus not collected from Río Zuñag Reserve I Pristimantis sp (DHMECN 16250 from El Encanto) . Photographs Juan Pablo Reyes Puig, Mario Yánez Muñoz, Jorge Brito and Lou Jost.
(Figs
Skin on dorsum finely shagreen with rounded tubercles widespread; venter areolate with some pustules, discoidal fold present; anal ornamentation absent, with several rounded tubercles; forearms slender with two subconical ulnar tubercles and a row of subconical tubercles along the anterior edge (reduced or less evident in preservation effects); fingers with fine lateral fringes, palmar tubercle oval, the same size and shape as thenar; subarticular tubercles rounded and defined, with supernumerary tubercles at the base of each digit; digital pads truncated and expanded, twice as wide as the digit in fingers III, IV, on fingers I and II slightly wider than digit; all fingers have digital pads defined by circumferential grooves (Fig.
Hind-limbs slender, tibia length 50.78% SVL, two subconical tubercles on the heel, a row of subconical tubercles on the outer edge of tarsus; inner tarsal fold present; toes with fine lateral fringes, without digital webbing, digital pads of the toes expanded, on toes IV and V twice as wide as digits and on toes I, II, III slightly more expanded than digit; low and rounded subarticular tubercles, supernumerary tubercles weakly defined and rounded; metatarsal tubercles present, inner oval three times the width of the outer tubercle that is rounded; toe V longer than III, not reaching to the base of distal subarticular tubercle of toe IV.
Colour of holotype in life (Fig.
Colour of holotype in ethanol 70% (Fig.
Variation (Fig.
Measurements (in mm) of type series of Pristimantis maryanneae sp. nov. and P. burtoniorum sp. nov.
Pristimantis burtoniorum sp. nov. | Pristimantis maryanneae sp. nov. | |||
---|---|---|---|---|
Characters | Females (n = 3) | Males (n = 3) | Females (n = 1) | Males (n = 3) |
SVL | 20.8–27.3 (23.4 ± 2.7) | 16.6–17.5 (17.1 ± 0.4) | 21.1 | 17.6–17.9 (17.8 ± 0.1) |
TL | 11.7–12.9 (12.4 ± 0.5) | 9.1–9.4 (9.3 ± 0.2) | 10.3 | 8.7–9.1 0(8.9 ± 0.5) |
FL | 10.2–10.8 (10.5 ± 0.2) | 7.8–8.8 (8.1 ± 0.4) | 9.4 | 7.9–9.2 (8.4 ± 0.5) |
HW | 7.4–8.5 (8.1± 0.5) | 6.2–6.5 (6.3 ± 0.2) | 8.9 | 6.1–6.8 (6.4 ± 0.3) |
HL | 8.7–9.4 (9.1 ± 0.3) | 6.7–7.7 (7.3 ± 0.4) | 8.0 | 6.9–7.3 (7.1 ± 0.2) |
IOD | 2.7–2.8 (2.7 ± 0.01) | 2.3–2.7 (2.4 ± 0.2) | 2.4 | 2.2–2.5 (2.3 ± 0.2) |
EW | 1.6–2.4 (1.9 ± 0.3) | 1.4–1.9 (1.7 ± 0.3) | 1.5 | 1.5–2.0 (1.8 ± 0.2) |
IND | 2.2–2.2 (2.2 ± 0.0.1) | 1.7–2.1 (1.8 ± 0.2) | 2 | 1.7–2.0 (1.8 ± 0.1) |
EN | 2.3–2.5 (2.4 ± 0.1) | 1.7–2.1 (1.8 ± 0.2) | 2.1 | 1.5–1.8 (1.7 ± 0.2) |
TD | 1.1–1.2 (1.1 ± 0.06) | 0.9–1.0 (0.9 ± 0.03) | 1.0 | 0.7–0.8 (0.8 ± 0.02) |
ED | 3.0–3.1 (3.0 ± 0.01) | 2.3–2.4 (2.3 ± 0.1) | 2.6 | 2.2–2.4 (2.3 ± 0.1) |
Pristimantis maryanneae is known only from the type locality, Naturetek Vizcaya Reserve, located at Ulba Parish, Baños township, Tungurahua Province, at 2400 m elevation in the eastern versant on the Andes in central Ecuador (Fig.
Specific epithet is in recognition of Maryanne Mills (née Sawle), a zoologist from Perth, Australia. In 1986, she helped her husband, David Mills, set up the UK’s premier wildlife tour operator, Naturetrek and she has been based in England ever since. Her passion for the environment and its conservation has led Naturetrek to donate widely to this cause, including donations to World Land Trust which allowed EcoMinga Foundation to purchase more than 1,000 acres of Ecuadorian cloud forest, where this new species of terrestrial frog was discovered.
Holotype. DHMECN 14479 (adult Female, Fig.
Paratypes (2 females, 3 males). DHMECN 14482 (♀), DHMECN 14447 (♀) y DHMECN 14480 (♂), DHMECN 14478 (♂), DHMECN 14481(♂), with same data as the holotype.
We assign the new species to Pristimantis, based on having head about as wide as body; tympanic membrane differentiated t; cranial crests usually; dentigerous process of vomers usually present; “S” condition of the adductor muscles; terminal discs on digits, bearing well-defined circumferential grooves, supported by T-shaped terminal phalanges; comparative lengths of fingers I and II variable; toe V as long as, or longer than, toe III; and subarticular tubercles not protruding; (Hedges 2008).
Pristimantis burtoniorum sp. nov. is distinguished from all congeners by the following combination of characters: (1) skin on dorsum and flanks finely shagreen with a slightly defined mid-dorsal fold, which extends from the tip of the snout to the ventre; skin on ventre areolate, dorsolateral folds absent; discoidal fold present and defined; (2) tympanum present; tympanic membrane and annulus present, equivalent to 25% of the eye diameter; with a single subconic postrictal tubercle; (3) snout large and subacuminate in dorsal and lateral profile; with several small subconic tubercles along the upper mandibulae, more evident in females; (4) upper eyelid with 3–4 large subconic tubercles; one subconic interorbital tubercle, followed by a row of rounded tubercles along middle of the snout; upper eyelid wider than interorbital distance; cranial crests absent; (5) dentigerous process of vomer present, oval in outline with 4–5 teeth oval; (6) males lacking vocal slits, nuptial pads weakly defined; (7) finger I shorter than II ; expanded digital pads, extended in fingers II-IV; two times the width of the digits; (8) fingers with large lateral fringes; (9) forearms with small conic ulnar tubercles; (10) heel with a small conic tubercle; outer border of the tarsus with small conical tubercles, inner tarsal fold present, weakly defined in the first portion; (11) two metatarsal tubercles, inner oval twice size of the outer tubercle that is round-shaped; (12) toes with fine lateral fringes; plantar supernumerary tubercles present, toe V larger than III, not extending further than distal subarticular tubercle of toe IV; (13) dorsal colouration grey with transversal marks dark brown, legs and arms with diagonal bands dark brown with interspaces pink (red in life), flanks with oblique bands finely delineated by cream, hidden surfaces of the venter and groin red; ventral colour grey dense, marked by dark brown, throat and outer mandibulae with dark brown marks, brown-red iris and (14) SVL in males 16.61–17.45 mm; females 20.81–27.03 mm.
Pristimantis burtoniorum is characterised by the presence of red colouration in hidden surfaces of the hind-limbs, this colouration combined with banded patterns of brown and pink. The presence of tubercles on the upper eyelid, interorbital tubercle and a row of rounded tubercles along snout to the tip and a pale red venter with dark brown mottled pattern in life, easily distinguish the new species from other congeners occurring on the eastern Ecuadorian Andes, diagnostic morphological characters avoiding polymorphism of previously-known species (Fig.
(Figs
Skin of the dorsum finely shagreen with scattered rounded tubercles; slightly defined dermal fold extending from the tip of the snout to the vent; venter areolate, discoidal fold present; without anal ornamentation and with low tubercles. Forearms slender with three lower ulnar tubercles and a row on the anterior region of the forearm, weakly defined or reduced by preservation effects, fingers with fine lateral fringes (Fig.
Hind-limbs slender, tibia length 56.7% snout-vent length, small subconic tubercle on the heel with a row of three lower tubercles; inner tarsal fold present, outer edge of the tarsus with low tubercles; toes with fine lateral fringes, without digital webbing, toes digital pads expanded to twice the width of the digit; subarticular tubercles rounded, well defined and elevated, small supernumerary tubercles weakly defined; metatarsal tubercles present, inner oval double in size than outer that is rounded; toe V much longer than III, reaching base of distal subarticular tubercle of toe IV.
Colour of holotype in life (Fig.
Colour of holotype in ethanol 70% (Fig.
Variation (Fig.
Pristimantis burtoniorum is known only from the type locality in the Machay Reserve, Rio Verde Parish, Baños township, Tungurahua Province, Republic of Ecuador (Fig.
Species epithet is the genitive plural of “Burton” in Latin, in recognition of John and Viv Burton, who founded and led the World Land Trust for most of its existence. Their impact on nature conservation is worldwide. Without the World Land Trust’s “Forests in the Sky” initiative, it would not have been possible for EcoMinga Foundation to establish the Machay Reserve and complete the Llanganates-Sangay Ecological Corridor.
The Upper Pastaza watershed shows a wide gradient of ecosystems, habitats and microhabitats for amphibian communities, with more diversity of species and reproductive strategies at eastern sites of study, mainly Bufonidae, Centrolenidae, Dendrobatidae, and Hylidae, highly influenced by Amazonian species groups and related to the availability of water resources for its reproductive modes, while western fauna appears to have more local endemism between localities north to south with dominant presence of Strabomantid frogs of the genus Pristimantis in montane and cloud forest localities; however, further research will complement our appreciation.
Our study found high species richness in terrestrial frogs and filled some gaps in the distributions of some Andean arboreal frog lineages. We found a high proportion of candidate new species, of which two are described in this article. Previous studies have confirmed the high endemism and richness of the Upper Rio Pastaza watershed, specifically in the Llanganates-Sangay Ecological Corridor (
Our post-hoc analysis showed that SVL had a potentially important relationship with elevation, but the SVL values are widely scattered and the parameters of the best-fit least squares line for log10 SVL as a function of elevation (in metres) have wide confidence intervals. One study investigating this same relationship, but within a population of a single species (in a very different habitat), showed a similar trend, with individuals decreasing in SVL by around 10% per thousand metres elevation change (
Despite our limitations, it is evident some examples of decreasing SVL with altitude in local communities of the study area, as an example, Bufonids genus Rhinella found in lower elevation sites, are larger and more slender than the Andean Osornophryne genus, with short SVL and limbs (Yánez-Muñoz et al. 2013). Another example could be addressed in the Pristimantis genus, with larger and more slender species in conspicillatus or lacrimosus groups in lower tropical zones, in comparison with smaller and short limbed species belonging to the Pristimantis myersi species group found in Andean ecosystems at high altitude (
Our initial studies of the amphibian diversity pattern in the Upper Rio Pastaza watershed found a high altitudinal turnover of species, in bands with elevation amplitude less than 600 m. There was high horizontal heterogeneity as well. Over a distance of less than 40 km in the watershed, three communities share only 25% of the composition of their batracofauna (Yánez-Muñoz et al. 2013).
At first, it may seem surprising that peaks such as Vizcaya and Machay, separated by less than 15 km in a straight line and both on the same side of the Rio Pastaza, connected by contiguous forest at elevations subject to this study, are so dissimilar from each other and that, in spite of the enormous barrier of the deep and dry canyon of the Rio Pastaza, they have more similarity to communities at the same longitude south of the Pastaza. For example, based on our study, the Naturetrek Viscaya Reserve is more similar to the Chamana Reserve on the opposite side of the Rio Pastaza than it is to the nearby Machay Reserve on the same side of the Rio Pastaza (Fig.
These results suggest that, while geographic barriers play a role in anuran distributions, an additional layer of complexity is added by small-scale spatial climate variations caused by the interaction of winds and topography; this distribution pattern has also been found in locally-endemic orchids, such as Lepanthes showing close relationship to the amount of precipitation (
While any specific microclimate may be patchy or isolated today, massive climate changes during the Pleistocene and Holocene almost certainly changed the topology of these patches, allowing the associated frogs to colonise new areas with the same microclimate, which later became isolated again as climate changed (
For fifteen years, we have collected and analysed information on amphibians in the Upper Rio Pastaza watershed and this has allowed us to establish species limits and describe several new lineages. However, we have refrained from issuing hypotheses on the evolutionary relationships of new species or making any deeper phylogenetic judgements. The present work will not be the exception. However, within our line of research, we can here announce a subsequent investigation that will summarise the phylogenetic, biogeographic and macro-ecological position of this diverse and poorly-known amphibian fauna of the tropical Andes.
We thank the donors who have made the creation of the Reserves possible, such as the World Land Trust and Naturetrek, as well as the Ecominga team of Javier Robayo, Fausto Recalde, Santiago Recalde, David Mesías Quinatoa Gaibor, Jesús Recalde, Jordy Salazar, Jorge Peña, Eduardo Peña and Stalin Peña for logistical support for the fieldwork and for their own observations of the frogs discussed here, as well as the Ministry of Environment for research permit No. 02-2018-IC-FAU-DPAT-VS and the framework agreement on access to genetic resources MAE-DNB-CM-2016-0045, MAE-DNB-CM-2019-0120. Lou Jost thanks John V. Moore for grants to the Population Biology Foundation in support of his work.
We also want to thank to the World Wildlife Found (WWF-Ecuador) and Hempel Foundation for its help to preserve the Llanganates Sangay Ecological Corridor as an important area for its unique biodiversity.
List of amphibians recorded in Naturetrek-Vizcaya and Machay Reserves (Number of species is show in parentheses)
Taxon Amphibia (23) | Absolute abundance 97 | Reserves: Machay Ecological Reserve (MR) and Naturetrek-Vizcaya Reserve (NVR) |
---|---|---|
BUFONIDAE (1) | – | – |
1. Osornophryne simpsoni | 4 | MR |
CENTROLENIDAE (1) | – | – |
2. Centrolene buckleyi complex | 1 | NVR |
HEMIPHRACTIDAE (1) | – | – |
3. Gastrotheca sp. | 2 | NVR |
HYLIDAE (1) | – | – |
4. Hyloscirtus sp. | 2 | MR |
STRABOMANTIDAE (19) | – | – |
5. Niceforonia sp. | 3 | MR |
6. Noblella naturetrekii | 3 | NVR |
7. Pristimantis bellae | 4 | MR |
8. Pristimantis buckleyi complex | 2 | MR |
9. Pristimantis eriphus complex | 8 | MR |
10. Pristimantis burtoniorum sp. nov. | 7 | MR |
11. Pristimantis maryanneae sp. nov. | 4 | NVR |
12. Pristimantis pastazensis | 1 | NVR |
13 Pristimantis tinguichaca | 1 | MR |
14. Pristimantis tungurahua | 7 | NVR |
15. Pristimantis aff. eriphus | 3 | MR |
16. Pristimantis aff. gladiator | 9 | MR |
17. Pristimantis aff. bicantus | 6 | MR |
18. Pristimantis aff. tungurahua | 1 | MR |
19. Pristimantis sp. A | 1 | MR |
20. Pristimantis sp. B | 6 | MR |
21. Pristimantis sp. C | 4 | MR |
22. Pristimantis sp. D | 12 | MR |
23. Pristimantis sp. E | 1 | MR |
List of Amphibians recorded in six localities of the Upper Pastaza Basin: Anzu Reserve (AR), Naturetrek-Cerro Candelaria Reserves (NCCR), Zuñac Reserve (ZR), Machay Reserve (MR), Naturetrek-Vizcaya Reserve (NVR), Chamana Reserve (CR).
TAXON AMPHIBIAN (92) | AR | ZR | CCR | MR | NVR | CR |
---|---|---|---|---|---|---|
AROMOBATIDAE (1) | – | – | – | – | – | – |
1. Allobates kingsburyi | x | 0 | 0 | 0 | 0 | 0 |
BUFONIDAE (5) | – | – | – | – | – | – |
2. Atelopus palmatus | 0 | x | 0 | 0 | 0 | 0 |
3. Rhinella festae | x | x | 0 | 0 | 0 | 0 |
4. Rhinella poepigii | x | 0 | x | 0 | 0 | 0 |
5. Rhinella margaritifera | x | x | x | 0 | 0 | 0 |
6. Osornophryne simpsoni | 0 | x | 0 | x | 0 | 0 |
CENTROLENIDAE (4) | – | – | – | – | – | – |
7. Chimerella mariaelenae | x | x | x | 0 | 0 | 0 |
8. Centrolene buckleyi complex | 0 | 0 | x | 0 | x | 0 |
9. Rulyrana flavopunctata | x | x | 0 | 0 | 0 | 0 |
10. Nymphargus cochranae | x | 0 | x | 0 | 0 | 0 |
DENDROBATIDAE (1) | – | – | – | – | – | – |
11. Ranitomeya variabilis | x | 0 | 0 | 0 | 0 | 0 |
HEMIPHRACTIDAE (2) | – | – | – | – | – | – |
12. Gastrotheca testudinea | 0 | 0 | x | 0 | 0 | x |
13. Gastrotheca sp. | 0 | 0 | 0 | 0 | x | 0 |
HYLIDAE (16) | – | – | – | – | – | – |
14. Dendropsophus bifurcus | x | 0 | 0 | 0 | 0 | 0 |
15. Dendropsophus bockermanni | x | 0 | 0 | 0 | 0 | 0 |
16. Dendropsophus parviceps | x | x | 0 | x | 0 | 0 |
17. Dendropsophus sarayacuensis | 0 | 0 | x | 0 | 0 | 0 |
18. Dendropsophus minutos | x | 0 | 0 | 0 | 0 | 0 |
19. Hyloscirtus phyllognatus | x | x | 0 | 0 | 0 | 0 |
20. Hyloscirtus sp. | 0 | 0 | 0 | x | 0 | 0 |
21. Boana almendarizae | x | x | x | 0 | 0 | 0 |
22. Boana cinerascens | x | 0 | 0 | 0 | 0 | 0 |
23. Boana geografica | x | 0 | 0 | 0 | 0 | 0 |
24. Boana lanciformis | x | 0 | 0 | 0 | 0 | 0 |
25. Osteceophalus fuscifacies | x | 0 | 0 | 0 | 0 | 0 |
26. Osteocephalus verruciger | x | x | x | 0 | 0 | 0 |
27. Osteocephalus mutabor | x | 0 | 0 | 0 | 0 | 0 |
28. Scinax ruber | x | 0 | x | 0 | 0 | 0 |
29. Trachycephalus cunauaru | x | 0 | 0 | 0 | 0 | 0 |
LEPTODACTYLIDAE (5) | – | – | – | – | – | – |
30. Adenomera andreae | x | 0 | 0 | 0 | 0 | 0 |
31. Engystomops petersi | x | 0 | 0 | 0 | 0 | 0 |
32. Leptodactylus andreae | x | 0 | 0 | 0 | 0 | 0 |
33. Leptodactylus lineatus | x | 0 | 0 | 0 | 0 | 0 |
34. Leptodactylus wagneri | x | 0 | 0 | 0 | 0 | 0 |
STRABOMANTIDAE (58) | – | – | – | – | – | – |
35. Niceforonia elassodisca | 0 | x | 0 | 0 | 0 | 0 |
36. Niceforonia nigrovittata | x | 0 | 0 | 0 | 0 | 0 |
37. Niceforonia sp. | 0 | 0 | 0 | x | 0 | 0 |
38. Nobella lochites | 0 | x | 0 | 0 | 0 | 0 |
39. Nobella naturetrekii | 0 | 0 | x | 0 | x | 0 |
40. Pristimantis altamazonicus | x | x | 0 | 0 | 0 | 0 |
41. Pristimantis altamnis | x | x | 0 | 0 | 0 | 0 |
42. Pristimantis ardyae | 0 | 0 | x | 0 | 0 | 0 |
43. Pristimantis bellae | x | x | x | x | 0 | 0 |
44. Pristimantis bicantus | 0 | x | x | 0 | 0 | 0 |
45. Pristimantis buckleyi complex | 0 | 0 | 0 | x | 0 | 0 |
46. 10. Pristimantis burtoniorum sp. nov. | 0 | 0 | 0 | x | 0 | 0 |
47. Pristimantis churuwiai | 0 | 0 | x | 0 | 0 | 0 |
48. Pristimantis croceoinguinis | x | 0 | 0 | 0 | 0 | 0 |
49. Pristimantis diadematus | x | 0 | 0 | 0 | 0 | 0 |
50. Pristimantis enigmaticus | 0 | x | 0 | 0 | 0 | 0 |
51. Pristimantis eriphus complex | 0 | x | x | x | 0 | x |
52. Pristimantis ganonotus | 0 | x | x | 0 | 0 | 0 |
53. Pristimantis galdi | 0 | x | 0 | 0 | 0 | 0 |
54. Pristimantis incomptus | x | x | 0 | 0 | 0 | 0 |
55. Pristimantis lanthanites | x | 0 | x | 0 | 0 | 0 |
56. Pristimantis loujosti | 0 | 0 | x | 0 | 0 | 0 |
57. Pristimantis marcoreyesi | 0 | 0 | x | 0 | 0 | x |
58. Pristimantis maryanneae sp. nov. | 0 | 0 | 0 | 0 | 1 | 0 |
59. Pristimantis modipeplus | 0 | 0 | 0 | 0 | 0 | 0 |
60. Pristimantis nigrogriseus | 0 | 0 | 0 | 0 | 0 | 0 |
61. Pristimantis pastazensis | 0 | 0 | x | 0 | x | x |
62. Pristimantis petersioides | x | 0 | x | 0 | 0 | 0 |
63. Pristimantis pinchaque | 0 | x | 0 | 0 | 0 | 0 |
64. Pristimantis prolatus | x | x | 0 | 0 | 0 | 0 |
65. Pristimantis puruscafeum | 0 | 0 | x | 0 | 0 | 0 |
66. Pristimantis quaquaversus | x | x | x | 0 | 0 | 0 |
67. Pristimantis rubicundus | 0 | x | 0 | 0 | 0 | 0 |
68. Pristimantis sacharuna | 0 | x | 0 | 0 | 0 | 0 |
69. Pristimantis tinguichaca | 0 | 0 | x | 1 | 0 | 0 |
70. Pristimantis tungurahua | 0 | 0 | x | 0 | x | x |
71. Pristimantis ventrimarmoratus | 0 | x | x | 0 | 0 | 0 |
72. Pristimantis w nigrum | 0 | 0 | x | 0 | 0 | 0 |
73. Pristimantis yanezi | 0 | x | 0 | 0 | 0 | 0 |
74. Pristimantis aff. bicantus | 0 | 0 | 0 | x | 0 | 0 |
75. Pristimantis aff. cajamarcensis | 0 | 0 | x | 0 | 0 | 0 |
76. Pristimantis aff. cremnobates | 0 | x | x | 0 | 0 | 0 |
77. Pristimantis aff. eriphus | 0 | x | 0 | x | 0 | 0 |
78. Pristimantis aff. gladiator | 0 | 0 | x | x | 0 | x |
79. Pristimantis aff. tungurahua | 0 | 0 | 0 | x | 0 | 0 |
80. Pristimantis grp. calcarulatus | 0 | 0 | x | 0 | 0 | 0 |
81. Pristimantis grp. conspicilliatus | x | x | x | 0 | 0 | 0 |
82. Pristimantis grp. devillei | 0 | 0 | x | 0 | 0 | x |
83. Pristimantis grp. >orcesi | 0 | 0 | x | 0 | 0 | 0 |
84. Pristimantis sp. A | 0 | 0 | 0 | x | 0 | 0 |
85. Pristimantis sp. B | 0 | 0 | 0 | x | 0 | 0 |
86. Pristimantis sp. C | 0 | 0 | 0 | x | 0 | 0 |
87. Pristimantis sp. D | 0 | 0 | 0 | x | 0 | 0 |
88. Pristimantis sp. E | 0 | 0 | 0 | x | 0 | 0 |
89. Pristimantis sp. F | 0 | x | 0 | 0 | 0 | 0 |
90. Pristimantis sp. G | 0 | 0 | 0 | 0 | 0 | x |
91. Pristimantis sp. H | 0 | 0 | 0 | 0 | 0 | x |
92. Strabomantis cornutus | 0 | 0 | 1 | 0 | 0 | 0 |