ZooKeys 1063: 23-48 (202 1) A peer-reviewed open-access journal

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Amphibians of the equatorial seasonally
dry forests of Ecuador and Peru

Diego Armijos-Ojeda'??, Diana Székely!?, Paul Székely'?, Dan Cogalniceanu’,
Diego F. Cisneros-Heredia**”*, Leonardo Ordéfiez-Delgado'?,

Adrian Escudero’, Carlos Ivan Espinosa'

| Laboratorio de Ecologta Tropical y Servicios Ecosistémicos (EcoSs-Lab), Departamento de Ciencias Biolégicas

y Agropecuarias, Universidad Técnica Particular de Loja, Loja 110107, Ecuador 2. Programa de Doctorado en
Conservacion de Recursos Naturales, Escuela Internacional de Doctorado, Universidad Rey Juan Carlos, 28933
Mostoles, Madrid, Spain 3 Museo de Zoologia, Universidad Técnica Particular de Loja, San Cayetano Alto,
calle Paris s/n, Loja, Ecuador 4 Faculty of Natural and Agricultural Sciences, Ovidius University Constanta,
900470, Constanta, Romania § Colegio de Ciencias Biolégicas y Ambientales COCIBA, Universidad San
Francisco de Quito USFQ, Quito 170901, Ecuador 6 Museo de Zoologia & Laboratorio de Zoologia Terrestre,
Instituto de Biodiversidad Tropical iBIOTROP Universidad San Francisco de Quito USFQ, Quito, Ecuador
7 Department of Geography, Kings College, London, UK 8 Instituto Nacional de Biodiversidad INABIO,
Quito, Ecuador 9 Department of Science, Rey Juan Carlos University, 28933, Moéstoles, Madrid, Spain

Corresponding author: Diana Székely (dszekely@utpl.edu.ec)

Academic editor: Luis Cerfaco | Received 7 June 2021 | Accepted 20 August 2021 | Published 18 October 2021
http://zoobank.org/7 CAAD4A9-4036-4199-B8CD-CC55557528C2

Citation: Armijos-Ojeda D, Székely D, Székely P, Cogalniceanu D, Cisneros-Heredia DE, Ordéfez-Delgado L,
Escudero A, Espinosa CI (2021) Amphibians of the equatorial seasonally dry forests of Ecuador and Peru. ZooKeys
1063: 23-48. https://doi.org/10.3897/zookeys.1063.69580

Abstract

Seasonally dry forests (SDFs) are one of the most challenging ecosystems for amphibians, fueling the di-
versity of this group of vertebrates. An updated inventory of native amphibians present in the Equatorial
SDF is provided, which extends along the Pacific coast of Ecuador and northwestern Peru. The study is
based on an extensive field sampling (two thirds of the total records) carried out throughout the Equatorial
SDE, along with a compilation of the available information on distribution of amphibians in the region
from published scientific papers, museum collections and on-line databases. The final dataset included
2,032 occurrence records for 30 amphibian species, belonging to eight anuran families. Additionally, data
regarding conservation status, habitat use, spawn deposition site, reproductive mode, and body size, along
with an identification key for all encountered species are provided. The results indicate a strong sampling

bias with a deficit in the Peruvian part of the study area, and a need for urgent inventories targeted at

Copyright Diego Armijos-Ojeda et al. 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.

24 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

under-sampled areas, using modern taxonomic methods. The study emphasizes the conservation priorities
in the Equatorial SDE, based on the distribution, conservation status and life-history data. This informa-
tion should be useful for the local authorities and institutions involved in the management and conserva-

tion of biodiversity in SDF.

Keywords

Annotated list, Anura, Conservation, Distribution, Herpetofauna, Life-history

Introduction

Seasonally dry forests (hereafter SDFs) have been recently recognized as a coherent
biome distributed across South America (Prado and Gibbs 1993; Pennington et al.
2000; Pennington et al. 2006; Linares-Palomino et al. 2011). They consist of tree- or
shrub-dominated ecosystems with deciduous or semideciduous vegetation, occurring
in frost-free areas with mean annual temperatures higher than 17 °C, high seasonal
rainfall that sums less than 1,600 mm/year, and at least 5—6 months annually with less
than 100 mm/month (Murphy and Lugo 1986; Pennington et al. 2000; Prado 2000;
Espinosa et al. 2012). Although animal diversity of Neotropical SDFs has received
relatively little attention (Sanchez-Azofeifa et al. 2005), a general trend of lower species
richness is apparent when compared to neighboring moister forest ecosystems such as
rainforests and cloud forests (Espinosa et al. 2011; Hanson 2011; Jenkins et al. 2013;
Guedes et al. 2018). This trend is quite evident in amphibians, organisms that are
highly dependent of humid conditions. The harsher climate conditions typical for the
SDF act as strong limiting factors for amphibian diversity (Duellman 1988; Székely et
al. 2016). Even so, survey efforts carried out in these habitats have revealed high levels
of amphibian endemism, and diverse behavioral and physiological adaptations allow-
ing most of these species to endure long periods of low food availability and hydric
stress (Ceballos 1995; Chazdon et al. 2011; Stoner and Timm 2011).

In the Neotropics, there are at least four distinct phytogeographic groups of SDF:
Caribbean-Mesoamerican, Ecuadorian-Peruvian, Brazilian Caatinga, and Central
South American (Prado 2000; Linares-Palomino 2004a). Among them, the Ecuado-
rian-Peruvian SDF has the smallest extent, aggregating coastal SDFs from western
Ecuador and northwestern Peru (Pennington et al. 2000; Peralvo et al. 2007), but
excluding the seasonal habitats from Huancabamba and Marafon, which, although
relatively close spatially, are considered to be biogeographically distinct due to the
fact that the Andes mountain-range represents a dispersal barrier (Linares-Palomino
2004b). Chapman (1926) was the first to recognize the high levels of biodiversity
and endemism of the Ecuadorian SDE, using the term Tropical Arid Fauna. Later, the
name Tumbesian Centre of Endemism has been extensively used (Cracraft 1985; Best
and Kessler 1995; Stattersfield et al. 1998) for this biogeographic region, recognized
as a center of endemism at a global scale taking into consideration the better studied
taxa, i.e., birds (Best and Kessler 1995) and vascular plants (Davis et al. 1997) and,

Amphibians of the equatorial seasonally dry forest 2

consequently, a global priority for conservation (DryFlor 2016) and a hotspot for bio-
diversity (Myers et al. 2000). Other authors have referred to this area under different
(complete or partially synonym) names: Ecuadorian Subcentre (Miller 1973), Guayas
Province (Ringuelet 1975), Ecuadorian Pacific Dry Forest (Udvardy 1975), Pacific
Equatorial Dominion (Ab’Saber 1977), Tumbesian Centre (Cracraft 1985), Ecuado-
rian Dry Forest and Western Ecuador Moist Forest (Dinnerstein 1995), Western Ec-
uador Province (Morrone 1999), Arid Ecuadorian and Tumbes-Piura Provinces (Mor-
rone 2001), Equatorial Pacific Area (Porzecanski and Cracraft 2005), Western Ecuador
and Ecuadorian Provinces (Morrone 2014), and there is currently a lack of consensus
about the precise position and extent of the SDF in Ecuador and Peru. ‘These diverse
definitions are usually based on endemism patterns of either vascular plants or birds, so
they tend to include neighboring moist habitats, ranging from mangroves to montane
cloud forests (Best and Kessler 1995), merging different ecosystems which are often
not characterized by seasonality. As a result, these delimitations are less effective when
applied to more water-dependent taxa such as amphibians, which show quite different
patterns of diversity and endemism.

The amphibian diversity in the SDF of the coastal areas of Ecuador and Peru has
been scarcely explored, with only a small number of localities being inventoried (Al-
mendariz and Carr 1992, 2012; Venegas 2005; Cisneros-Heredia 2006; Armijos-Ojeda
and Valarezo 2010; Amador and Martinez 2011; Székely et al. 2016; Sanchez-Nivicela
et al. 2015; Cuadrado et al. 2020). Several factors influence this lack of information,
including bias caused by researchers’ preference for the more biodiverse tropical rain
and cloud forests, logistic limitations imposed by site accessibility, and the short and
unpredictable rainy season when amphibians are active and can be detected.

The first step in the development of any effective management and conservation
strategy for amphibians is the completion of regional inventories, especially in the
context of rapid biodiversity loss and climate changes. Understanding species distri-
bution is especially urgent in the case of amphibians, the most threatened vertebrate
group worldwide (Catenazzi 2015). In this context, our aim was to update the list
of amphibian species and their distribution in the coastal SDF of Ecuador and Peru,
through extensive fieldwork and the compilation of all available information, to pri-
oritize conservation actions, promote public awareness and focus further inventory
efforts towards areas where gaps remain.

Materials and methods

Study area

For the purpose of the study, we use the definition of the Ecuadorian Province (Mor-
rone 2014), including all seasonally dry forests (SDFs) in this biogeographical region
and excluding neighboring moist habitats that are likely to promote amphibian com-
munities of different origin and with different characteristics. Henceforth, we will use

26 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23—48 (2021)

the term Equatorial SDF for this area, which has a finer resolution than the one of
Ecuadorian Province; also, we consider the term to be more adequate to denominate
territories in both Ecuador and Peru. To generate the map layer used in the analysis,
we used Quantum GIS (QGIS) environment 3.4.13 (QGIS.org 2021). To delimit
our study area, we used as a basis the national digital maps of ecosystem types for Ec-
uador (MAE 2013) and Peru (MINAM 2019). These two cartographic databases are
currently the most precise available for the area, due to their spatial resolution (scale
1:100,000). In both cases, the ministries of environment in the respective countries
define the types of ecosystems according to vegetation cover, bioclimate, biogeogra-
phy, physiography, altitude, and land use cover. The final map for the Equatorial SDF
included ecosystem types with a characteristic of seasonal distribution of precipitation
and a semi-deciduous and deciduous vegetation (forests, shrublands), and excluded the
Marafion dry forests (Suppl. material 1: Table $1). We added the “Anthropical” and
“No data” categories situated in areas of historical distribution of those ecosystems. The
resulting shape was manually corrected, fixing geometry problems and filling gaps with
the dedicated tool of QGIS to reduce the noise and obtain a more accurate area. The
final area covers 55,680.5 km? (of which 36.5% in Ecuador and 63.5% in Peru), with
an altitudinal range between 0 and 1631 ma.s.l., and consists of a narrow band (3-—
150 km wide) bordering the Pacific Ocean, extending from the Ecuadorian province
of Esmeraldas in the north, to the Peruvian department of Lambayeque in the south.

The climate in the Equatorial SDF region is characterized by a striking seasonal-
ity, with a dry season lasting between five and eight months (Escribano-Avila 2016),
a fairly stable high temperature throughout the year, and annual rainfall varying be-
tween 500—1,500 mm, while the average monthly rainfall varies between 10 mm to
more than 200 mm (Murphy and Lugo 1986; Espinosa et al. 2012). The vegetation is
dominated (>50%) by deciduous or semi-deciduous trees. The region is delimited by
neighboring ecosystems characterized by a higher rainfall input, such as the transition
zones to the Andean mountain range (foothills) in the eastern region and transition
zones to the Choco rainforest in the north.

Data collection

The distribution records were compiled from the following sources:

1. Field surveys. Field data were collected and geo-referenced by the authors be-
tween 2000 and 2021. Sampling was carried out at various locations (Fig. 1 — Field data),
using visual / auditory encounter surveys and active searches (Heyer et al. 1994). Spe-
cific methodologies varied, but consisted in both diurnal and nocturnal extensive surveys
carried out mainly during the rainy season, and included searches of suitable terrestrial
refugia, netting, torching, pitfall traps and call surveys, unconstrained by time or area.

2. Literature review. We carried out search routines between January and April
2021 on the online search engines Google Scholar (https://scholar.google.com/), Sci-
eLO (https://scielo.org/), Web of Science (http://webofknowledge.com/), retrieving

Amphibians of the equatorial seasonally dry forest af

papers by using the following search terms: “amphibian”, “Anura’, “herpetofauna’,
and “Tumbesian”, “Ecuadorian dry forest”, “Peruvian dry forest”, and reviewing the
first 200 results for each search. We included articles in peer-reviewed journals, as well
as theses and reports that included relevant information regarding the species distribu-
tion, where locations were either geo-referenced or precise enough to permit the assig-
nation of coordinates, and identification was done to species level (Fig. 1 — Literature).

3. Museum biological collections housed at Instituto Nacional de Biodiversidad,
Quito, Ecuador (DHMECN), and Museo de Zoologia, Universidad San Francisco de
Quito, Ecuador (ZSFQ).

4. Publicly available species distribution data on the Global Biodiversity Infor-
mation Facility (https://www.gbif.org/), which includes the iNaturalist platform data,
accessed April 2021 (https://doi.org/10.15468/dl.55dnar). These data were manually
curated, removing all vague locality descriptors, likely erroneous species identification,
and exotic species records (Zizka et al. 2020). We also filtered for duplicated records
(same species at the same coordinates at the same moment).

Regardless of source, we standardized the species list using the taxonomy of Am-
phibian Species of the World (Frost 2021). Only specimens that could be identified
to species level were included in the dataset. Non-native species records were removed
(ie., the bullfrog Lithobates catesbeianus). For each species, we indicate the extinc-
tion risk status at the global level based on the IUCN Red List of Threatened Species
(IUCN 2021).

To characterize species life-history traits, we carried out a literature search for each
species in peer-reviewed articles or books and completed with field observations when-
ever available (Suppl. material 2). We selected four relevant traits which reflect eco-
logical strategies, niche, and functional roles in the ecosystem (Oliveira et al. 2017)
and adopted some rather coarse categories to accommodate for the lack of ecological
information for most of the species present in the region. Species habitat use, defined
as the overall vertical foraging stratum preferred by the adult, resulted in four broad
categories: terrestrial/fossorial (foraging mostly on the ground or in leaf-litter, galler-

7a

Figure |. Distribution of amphibian occurrence records in the Equatorial Seasonally Dry Forest (SDF).
Maps are provided depending on the data source: Field data, Literature, Museum, Database.

28 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

ies, crevices, or holes on the floor), arboreal (predominantly perching on leaves in
trees, bushes, phytotelmata, grasses, including riparian vegetation), terrestrial/riparian
(found in terrestrial habitats close to or around bodies of water), and aquatic/riparian
(semi-aquatic species living in streams or ponds). We also reported the reproductive
mode (either larval or direct development), as well as the spawn site, the microhabitat
where eggs are deposited (either aquatic, terrestrial, or arboreal). As a morphologi-
cal character, body size was defined as the maximum snout-vent length (SVL) value
known for the species, and we report the value separately for females and males. Fi-
nally, we generated an identification key, based on morphological characters. However,
it is worth mentioning that in some taxa (e.g., the case of Engystomops spp.) the reliable
identification usually requires additional information (such as mating calls).

Specimen collection

In the case of voucher specimens, individuals were photographed, after which they were
euthanized using 20% benzocaine, fixed in 10% formalin, and stored in 70% ethanol.
Tissue samples for genetic analyses were preserved in 96% ethanol. Specimens are depos-
ited at Museo de Zoologia, Universidad Técnica Particular de Loja (MUTPL), and Museo
de Zoologia, Universidad San Francisco de Quito (ZSFQ) Ecuador. Information on these
specimens is included as field data since it was generated by the authors during fieldwork.

Research permits were issued by Ministerio del Ambiente del Ecuador. ‘This study
was evaluated and approved by the Ethics Committee of Universidad Técnica Particu-

lar de Loja (UTPL-CBEA-2016-001).

Results

The final dataset consists of 2,032 distribution records spread throughout the Equato-
rial SDF region. Seventy-seven records are from Peru, and 1,955 are from Ecuador
(Fig. 1). Our field records constitute most of the data points (Fig. 1 — Field data), i.e.
1,374 records (67.6%). The literature revision produced 285 records (14%) from 29
publications (Fig. 1 — Literature), while the museum collections of INABIO and ZSFQ.
included 87 records (4.3%, Fig. 1 - Museum). The online databases GBIF and iNatural-
ist contributed 286 data points, representing 14.1% of the dataset (Fig. 1 — Database).

Overall, we report 30 amphibian species for the Equatorial SDE, belonging to 14
genera and eight families (Figs 2—G); all 30 species were present in Ecuador, of which
16 were also encountered in Peru (Suppl. material 1: Table 2S). The best represented
family was Leptodactylidae (genera Engystomops and Leptodactylus) with eight species.
Five species (Ceratophrys stolemanni, Engystomops montubio, E. puyango, E. randi and
Lithobates bwana) are endemic to the Equatorial SDF. Two, Epipedobates anthonyi and
Leptodactylus labrosus, have a distribution mostly restricted to the Equatorial SDE, with
few occurrences in adjacent habitats, characterized by higher humidity/altitude. The
remaining 23 species have a wider distribution.

Amphibians of the equatorial seasonally dry forest Zo)

sk a ee

Figure 2. Amphibian species of the Equatorial Seasonally Dry Forest A Rhinella alata (photo by Sil-
via Aldas, https://bioweb.bio) B Rhinella horribilis C Hyalinobatrachium tatayoi D Ceratophrys stolemanni
E Epipedobates anthonyi F Epipedobates machalillaG Hyloxalus elachyhistus A Hyloxalus infraguttatus \ Boana
pellucens J Boana rosenbergi K Scinax quinquefasciatus L Scinax sugillatus (photograph by Santiago R. Ron,
https://bioweb.bio) M Scinax tsachila N Smilisca phaeota O Trachycephalus jordani P Trachycephalus quad-
rangulum Q Engystomops guayaco R Engystomops montubio S Engystomops pustulatus T Engystomops puyango
U Engystomops randi N Leptodactylus labrosus W Leptodactylus melanonotus XK Leptodactylus ventrimaculatus
Y Barycholos pulcher Z Pristimantis achatinus AA Pristimantis lymani AB Pristimantis subsigillatus AC Pristi-
mantis walkeri (photograph by Santiago R. Ron, https://bioweb.bio) AD Lithobates bwana. Habitat seasonal
change (Reserva Ecoldgica Arenillas) AE april (rainy season) AF december (dry season).

30 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

Regarding the global extinction risk status (IUCN 2021), one (C. stolzmanni) is
classified as Vulnerable, and three are Near Threatened (£. anthonyi, Hyalinobatra-
chium tatayoi, and Hyloxalus infraguttatus). Two are Data Deficient (Rhinella alata and
Engystomops guayaco) and another three (R. horribilis, Scinax tsachila and Trachycepha-
lus quadrangulum) are currently Not Evaluated, while the remaining 21 species have a

Least Concern IUCN status (Table 1).

Life-history characteristics

In terms of amphibian species habitat use, 17 (56.7%) are terrestrial / fossorial, nine
(30%) are arboreal, two are aquatic / riparian (6.7%), and two are terrestrial / ripar-
ian (6.7%) (Table 1). Most species have larval development (25 species, 83.3%), and
the five species of Strabomantidae have a direct development (16.7%). Amphibians
living in Equatorial SDF exhibit several reproductive strategies for egg deposition; the
most common behavior was to deposit eggs directly in the water (17 species, 56.6%,
amongst which the five Engystomops species which produce foam nests), terrestrial dep-
osition (12 species, 40%), and one species lays egg clutches on leaves overhanging water
(Hyalinobatrachium tatayoi). The range of body sizes is wide, with maximum adult size
varying between 16 mm (Epipedobates machalilla) and 130 mm (Rhinella horribilis).

Changes in distribution range

We report here the extension of the distribution ranges of four amphibian species de-
tected during fieldwork.

Ceratophrys stolzmanni (Pacific horned frog). This species is endemic to the low-
land Equatorial SDF (Ortega-Andrade et al. 2021), with a distribution extending
from its type locality, Tumbes, Peru (Steindachner 1882), in the south, up to La
Seca (Manabi, Ecuador), in the north. Distribution follows the Pacific coast, the in-
nermost point being 50 km from the coast (Cuadrado et al. 2020), but all previously
recorded locations were at low altitudes (up to 130 maz.s.l.). In the present study, we
extend the known distribution of this species by adding several new locations (Fig.
3). Amongst them, the record from Manabi, Ecuador (1.0679°S, 80.8308°W), in the
vicinity of the El Aromo oil refinery, at 380 m a.s.l., is the highest altitude reported
for the species. We also encountered the Pacific horned frog in Progreso, Reserva Ca-
zaderos (4.0259°S, 80.4497°W, 221 ma.s.l.) and Mangahurco, Area de Conservacién
Municipal Los Guayacanes (4.1611°S, 80.4388°W, 360 ma.s.l.), these being the first
records for the Loja province (Ecuador). They also represent the most continental
records for this species, being located at more than 70 km from the Pacific coast.
Another important observation is that the locations in Loja province, despite being
spatially close to the Tumbes region, are actually separated by the Cerro de Amotape
mountain range, which was until now considered a barrier for this typically lowland,
burrowing amphibian.

Amphibians of the equatorial seasonally dry forest 31

Table |. Life-history characteristics and conservation status for the amphibians of the Equatorial Season-
ally Dry Forest. IUCN Status — extinction risk status according to IUCN (2021): NE - Not Evaluated,
DD - Data Deficient, LC - Least Concern, NT - Near Threatened, VU - Vulnerable. Reproductive modes:
LDvy - Larval Development, DDv - Direct Development. * indicates species with a distribution restricted

to Equatorial Seasonally Dry Forest. References are given in Suppl. material 2. FD - unpublished informa-

tion collected by the authors during fieldwork.

a r) 8 8
> g a F 2 4,385 :
= zs D & 2 83 9259 5
E Z fc es BEES ES é
¥ Ss - So & gees ee
= e s~-s¢
Bufonidae Rhinella alata DD Terrestrial / fossorial Aquatic LDv 43.3 56.2 FD; (1)
Rhinella horribilis NE Terrestrial / fossorial Aquatic LDv 130.0 160.0 — FD; (2); (3); (4)
Centrolenidae Hyalinobatrachium tatayoi NT Arboreal Arboreal LDv 26.8 31.1 FD; (5); (6)
Ceratophryidae Ceratophrys stolemanni* VU | Terrestrial / fossorial Aquatic LDv 70.4 75.9 FD; (7); (8); (9)
Dendrobatidae Epipedobates anthonyi NT _ Terrestrial / fossorial Terrestrial LDv 25.0 27.0 FD; (10); (11)
Epipedobates machalilla LC _ Terrestrial / fossorial Terrestrial LDvy 16.0 17.6 FD; (12); (13)
Hyloxalus elachyhistus LC = Aquatic / riparian ‘Terrestrial LDv 24.1 24.8 FD; (12); (14)
Ayloxalus infraguttatus NT | Terrestrial / fossorial Terrestrial LDv 20.5 23.4 FD; (12); (15); (16)
Hylidae Boana pellucens LC Arboreal Aquatic LDv 52.9 61.0 (17); (18); (19);
(20); (21); (22)
Boana rosenbergi LC Arboreal Aquatic LDv 90.0 93.2 (19); (23); (24); (25)
Hylidae Scinax quinquefasciatus LC Arboreal Aquatic LDv 38.2 38.9 (26); (27)
Scinax sugillatus LC Arboreal Aquatic LDv 42.0 45.5 (27); (28)
Scinax tsachila NE Arboreal Aquatic LDvy 34.2 36.4 FD
Smilisca phaeota LC Arboreal Aquatic LDv 66.0 78.0 (29)
Trachycephalus jordani LC Arboreal Aquatic LDv 95.4 111.3 FD; (28); (30)
Trachycephalus quadrangulum NE Arboreal Aquatic LDv 76.9 80.8 FD; (28); (31)
Leptodactylidae Engystomops guayaco DD Terrestrial / fossorial Aquatic LDv 19.38 20.98 FD
Engystomops montubio* LC Terrestrial / fossorial Aquatic LDv 22.8 19.71 FD
Engystomops pustulatus LC Terrestrial / fossorial Aquatic LDv 32.3 36.5 FD
Engystomops puyango* LC Terrestrial / fossorial Aquatic LDv 30.5 32.6 FD; (13); (32)
Engystomops randi* LC Terrestrial / fossorial Aquatic LDv 18.7 19.7 (13); (33)
Leptodactylus labrosus LC Terrestrial / fossorial Terrestrial LDv 67.4 71.2 FD; (34); (35); (36)
Leptodactylus melanonotus LC Terrestrial / riparian Terrestrial LDv 43.4 48.1 (35); (37); (38)
Leptodactylus ventrimaculatus LC Terrestrial / riparian Terrestrial LDv 55.4 59.3 FD
Strabomantidae Barycholos pulcher LC Terrestrial / fossorial Terrestrial DDv 26.9 30.5 (39); (40)
Pristimantis achatinus LC Terrestrial / fossorial Terrestrial DDv 36.2 46.1 (19); (41); (42)
Pristimantis lymani LC Terrestrial / fossorial Terrestrial DDv 45.3 72.9 FD; (43); (44)
Pristimantis subsigillatus LC | Terrestrial / fossorial Terrestrial DDv 28.5 33.4 ED; (45)
Pristimantis walkeri LC Terrestrial / fossorial Terrestrial DDv 18.5 25.3 FD
Ranidae Lithobates bwana* LC Aquatic / riparian Aquatic LDv 63 95 FD; (46)

Engystomops puyango (Puyango dwarf frog). This small amphibian was recently de-
scribed from the Puyango Petrified Forest, in south-western Ecuador (Ron et al. 2014),
and was until now known from a small number of localities. We contribute several new
reports in the region; its presence in Casacay (3.3383°S, 79.7268°W, 146 ma.s.L.), El
Oro province, more than 72 km from the type locality, constitutes the farthest record
from the known distribution (Fig. 4).

Engystomops randi (Rand’s dwarf frog). Another recently described leptodactylid

species, which has a wider distribution, encompassing most of the Equatorial SDF

52

Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

close to the coast (Ron et al. 2014). We report for the first time its presence in Peru,
Tumbes Reserve (3.7743°S, 80.2249°W, 53 m a.s.l.) (Fig. 4).

Trachycephalus quadrangulum (Chocoan milk frog). This is a large tree frog,

mostly known from the coastal Ecuadorian region (Ron et al. 2016). We con-

tribute a new locality for Loja province in Ecuador, close to Bolaspamba

(4.1823°S, 80.3692°W, 416 ma.s.L.) (Fig. 5).

Key to the amphibian species of the Equatorial seasonally dry forests of
Ecuador and Peru

Qo |

ise

IDigite tips netiexpanGed nce wk stlasl, tesiss Meade reese sMay es iee tackle te ie bates Neate 2
FOTO TESS TE SPAIN EC altrerd arc aindeerconicAbeme inde tgbasree ttt dete nites sntenbe matacvdomindaeapowebanegt 13
Keratinized metatarsal spade present; extremely wide head and mouth.........
nimssienB sel estab sachet bn usle onesie np shone ne toutdnaa stats Mears Ceratophrys stolemanni

Keratinized:metatatsalespace-absentenc tus nt SO RA ie cette ee ace clatter 3
Parotid: Glatids: Present veccactevccses sencenssececeenigecevunte ben sveiaidesue veces winced uvengeeceetees 4
PRArOt@IG "lA ASADSENY sits tucta elas euaess. colsmet densa tudeas sets ias eoeabssetaenng rahBaaeul 10
Cranial crests present; adults medium or large: SVL > 40 mm; flank glands
ALSO it chat ale bce chats etoc enh dee Sue seete dea MicNtcces cane Mae soa lee don Rdlitern ine Cece 5

Cranial crests absent; adults small: SVL < 40 mm; flank glands present...... 6
Large sized, SVL of adults > 70 mm; parotoid glands large; tarsal fold pre-
SE MME cease oath aa Sota ah neat ce toch ee std ce eesdtae esti meee ter he tionseoeemese ree Rhinella horribilis
Medium sized, SVL of adults < 60 mm; parotoid glands small; tarsal fold
ALY SOE Mitesh Asuna asus ote eta AteMa etrs ban alta Mu taicnsui ATs uted Rhinella alata
SVL of adults:>+23-mms laceral:fringeés.on toesabsenit +. 20.0 f-.c0¢sncetpee onees vi
SVL of adults < 23 mm; lateral fringes on toes present... .eeeeeseeeeeeeeeeeeee 8
SVL of adults > 25 mm; larger tubercles on the dorsum ....... eee eeeeeeeeeeeeeees
i Aint slices ed pastes bates teapnatact oink Bane eens dbaamaee as, Engystomops pustulatus
SVL of adults > 23 mm; smaller and fewer tubercles on the dorsum.............
UR te ene serie oer 2. ee re we Wa ewe rh Weare Seer Ah Wee Engystomops puyango
SVL of adults 15—20 mm; lateral fringes on toes broad; webbing between toes
BiaSANs necn cust Nowkce acc lon teu Aiton Soak shctace Sac Minolta Deacsane Engystomops guayaco
Lateral fringes on toes narrow, webbing between toes absent........... eee 9
SVL of adults 17—22 mm; proportionately shorter flank and parotoid glands
seca gaten eeu te catgwvn ese Pou kceedan cau Cde cut bce out hla deat tial oh te Engystomops montubio
SVL of adults 17-20 mm; proportionately longer flank and parotoid glands

LEAP ARDS SIE te nS NR NDE AER AI Engystomops randi
Extensive webbing between the toes; subarticular tubercles low .................
Be awh sae ete aro ee tea cee eee ane, Bera ae Lithobates bwana
Webbing between the toes absent; subarticular tubercles well developed...11
Males with black horny thumb spines; toes with well-developed lateral fring-
Ssh seh lhe see IY as BE cadens t lh dh CAR ta Ms ic cee Leptodactylus melanonotus
Males without thumb spines; toes without developed lateral fringes ......... 12

12

Amphibians of the equatorial seasonally dry forest 33

Posterior surface of tarsus with many white tubercles; sole of foot with white

Ld 813) ce cc nae Sod Bria Ung ear we aeeeryyT Leptodactylus ventrimaculatus
Posterior surface of tarsus usually without white tubercles; sole of foot usually
Mele CW HLS CUD CECLES fad sni toe rtashne bhastnn shared shaghceutaue Leptodactylus labrosus
Expanded discs bearing a pair of scute-like fleshy structures on the dorsal
EY Thm b2ve ko) BCG CA oa | 0 yo Ree NOIRE OR Peon Cle Son EE ERO 14
Expanded discs without dorsal scute-like fleshy structures on tips of digits... 17
Broad, light middorsal stripe present............ eee Epipedobates anthony
ISG Farag eSeU URS Wr 67 te] 6) ot 0 pes i ea nt cae ERs 15
Venter immaculate (without white spots).............. Epipedobates machalilla
BS OY) ge alld Nd OT ey 0] Ro a OT 8, MR Le Ae eT 16
Extensive webbing between the toes.........ceceeeeeeeeees Hyloxalus elachyhistus
Limited webbing between the toes...........esseeeeseeeee Hyloxalus infraguttatus
Venter transparent with the white peritonea and lungs visible, dorsal surfaces
ereen With VellOw-SPOts:. sie cleserdwrsermeveeeeteeare Hyalinobatrachium tatayoi
Venter not transparent and internal organs not visible, dorsal surfaces brown,
PLC VE ORT CEM tow sanesins Coase niestanene vatewnsattoan'g aeSanh tunel Nein asa unehs ERneeeduNIaeg eI. katt 18
RingerstackinerWe pba: 4412.0. Letd essa ctatas Wats vanoellal heehee ds Animales 19
Webbing present between Tigers: tncduiecseusiseechevecbenveeunedeedaiebacailven cain 26
Toe II longer than Toe V; digit tips just slightly expanded (swollen); well
defined white glands posterior to angle of jaw............. Barycholos pulcher
oe N lonieer that iy Te WW 25 ececetercu ces nev cesteel Loy po testes Preven pete ong Per'sadoentisnderteaest 20
Himes lac kin@rex tensive WEDDING $5. tos Htastpstisels an soehichtencoisiesueation side asseseeuaes 21
NWeb bia Presel te Dec Wem tee s.0s sncsac bu, se csneeheh snot esan Ses tea ie wa on eetnas 24
Finger I longer than Finger II; dorsolateral folds present ....... cies 22
Finger I shorter than Finger II; dorsolateral folds absent ........ eee eee 23

Discs on fingers relatively small; inner surface of tarsus bearing long fold;
posterior surfaces of the thighs black with white spots or reticulations; SVL
OF Ales D573 AT os ih Sas aches eencaasiaie diet seadkdunenens svedes Pristimantis lymani
Discs on fingers broad; inner tarsal tubercle small; posterior surfaces of the
thighs brown with small cream flecks; SVL of adults 23-46 mm... ee
Bene ers ee oe ae ne ee Fen Lenore. Lean Pristimantis achatinus
Snout bearing papilla at tip; heel with small conical tubercle; SVL of adults

TES SATIN poe tetncah on eh tates ane aeae eae eek denen oe Pristimantis subsigillatus
Snout without papilla at tip; heel lacking tubercles; groin black with yellow
Spatss SW Lraiadults: 1325 aaa az cloner taeda dint teahien tee Pristimantis walkeri

Lower jaw with a row of tubercles; snout long; black and blue mottling in the
groin and on the anterior and posterior surfaces of the thighs... Scinax sugillatus

lower jawiwithouta-row, of tubercles. aise n,n accree teeth az peer eee 25
Shank bones visible through the skin, white to bluish-white; dorsum with
scattered to abundant small tubercles... Scinax quinquefasciatus

Shank bones visible through the skin, green; dorsum without tubercles........
Phe Re Reh ds Wy OP a eR eS AU ec NGne 2 BEEN, Belin ele Scinax tsachila

34

Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

Top of the head co-ossified and rough (integumentary-cranial co-ossified
skull); iris golden with irregular black spots; SVL of adults 65-111 mm.......
Me eee at ev egy een ev goer can en gues gus oe gu elute ose Re Trachycephalus jordani
Toptomithie-Reackira bear OssihGd f5.cptate: tients eased ct tae nade Seon ce sect eae es 27
Skin on dorsum tuberculate; webbing between the fingers extensive; dorsal
colorationsusually browns icae. .nipeecsr -nteusitunescrapteeeeune ats Boana rosenbergi
Skin on dorsum smooth; webbing between fingers basal to moderate....... 28
Pronounced calcar on the heel; webbing between the fingers moderate; dorsal
coloration usually green; iris yellowish .......... es eeeeeeeeeeeeees Boana pellucens
@aleair-on; celal Seite seis ome ees ela: Fas. en Seles ir a Sats eae eee 29
Webbing between the fingers moderate; iris golden with irregular black spots;
thick, glandular skin on the head and back. Trachycephalus quadrangulum
Webbing between the fingers basal; characteristic dark postorbital mark and
5 of AW LEcel E10} Ec Lac nt be eee Ts ail BE Reh es ee Smilisca phaeota

Clave para las especies de anfibios del bosque estacionalmente seco Ecuato-
rial de Ecuador y Peru

Qo |

XN

Hérminaciones-de los dedos-no-ex pandidassiciss..2eec.eevcccseotectbeseiuties davvetentts 2
Hernaiiactonrd €1Ostded osex panadidas were ntae a. tee eee setas et eee eae 13
Presencia de espadices metatarsiales queratinizados; cabeza y boca extremada-
MVE ESPATCNAS Ae vztece roa th vudt mn ron acunsustornetonstas testes teteat Ceratophrys stolemanni
ES PACCCoMETALALSI Ale MCEATINIZAAO*AUISEMIEE 5, sha.th ohssc toa cant Ponoesshos Shak Pusstcnn dhe 3
Presenicia:de cl anculassparObrOieleas s.o:.uss. Sees vsustshsees Rosettes lta eete oseakee SeNieants 4
Glandulas: parotoideas ausentes:muh sz ets. ees Ses ee eee ee 10
Presencia de crestas craneales; adultos medianos o grandes: LHC > 40 mm;
Blair ulasrdie ls HanCoyaUsciibes és: secre. x atten et cn Sarsed Wes saatuctscanbente attest yeetecae 5
Crestas craneales ausentes; adultos pequefios: LHC < 40 mm; glandulas del
HANG Os PECSCTLES wats. tats hea are ecu t es. cae ec taeda aR ets Mes 6
Tamanio grande, LHC de adultos > 70 mm; glandulas parotoideas grandes;
PLETE APA PEE SEIEE ccxeminds nop aadi one veumaronesdfinabntonsbastundes Rhinella horribilis

Tamafo mediano, LHC de adultos < 60 mm; glandulas parétidas pequefas;
Pulse Wear sal AUS eat. ences nade ema ton Eakon ch adel ones Rhinella alata
LHC de adultos > 23 mm; flecos laterales en los dedos de los pies ausentes......7
LHC de adultos < 23 mm; flecos laterales en los dedos de los pies presentes.... 8
LHC de adultos > 25 mm; tubérculos mas grandes en el dorso....... ees

ects nian at cath evagcca oa eatecmana a eee eau ws tose eM eecconaeRc Aas se raat Engystomops pustulatus
LHC de adultos > 23 mm; menos tubérculos y de tamafio menor en el
ORS OR fase ee ee, geen ea PEO os Engystomops puyango

LHC de adultos de 15 a 20 mm; flecos laterales en los dedos de los pies an-
chas; membrana entre los dedos de los pies basal........ Engystomops guayaco
flecos laterales en los dedos del pie estrechos; membranas entre los dedos del
POV CALISC UGS 8a, Pale oan net ese seach aS teeats daeseon toe rab ssbaes alee eeeauastendee eeeeniemens de eoments 9

20

Zl

Amphibians of the equatorial seasonally dry forest 35

LHC de adultos de 17 a 22 mm; glandulas parotoideas y del flanco propor-

cionalnrentesmas pequienast.We...4....ueten cele tual Engystomops montubio
LHC de adultos de 17 a 20 mm; glandulas parotoideas y del flanco propor-
CiOIal MEN te CIS ATCA AL, ats latuchuses sha lookiahiacelonens Engystomops randi
Extensas membranas entre los dedos de los pies; tubérculos subarticulares
Deh Soe RE a Se eet Lithobates bwana
Membranas entre los dedos de los pies ausentes; tubérculos subarticulares
bien.desarrolad oes cce uu A cle ere eee eee ee! 11
Machos con espinas corneas negras en los pulgares; dedos de los pies con
flecos laterales bien desarrollados.............eeeee Leptodactylus melanonotus
Machos sin espinas pulgares; dedos de los pies sin flecos laterales desarrol-
PCE SEs 2 toe lret nest ha teed nee ol mre en reed ema ea te ae arama 12
Superficie posterior del tarso con muchos tubérculos blancos; planta del pie
conrtuberculos, blancOs..s28..csussis< Ssctadeasee Leptodactylus ventrimaculatus
Superficie posterior del tarso generalmente sin tubérculos blancos; planta del
pie generalmente sin tubérculos blancos................ Leptodactylus labrosus

Discos expandidos que llevan un par de estructuras carnosas en forma de
escudos en la superficie dorsal de las puntas de los dedos ....... eee eeeeeeeeeee 14
Discos expandidos sin estructuras carnosas en forma de escudos dorsales en
TaSypUtinkas ClelOstcledOs tenga tere eeu Sasa ntae a sal ee eon Ae eee eee 17
Presencia de-unaiftanja-media‘dorsaltclata y-ainchaa i.) spas siento deteeatnetavbaces

Prarijatimiediave otsaltavise tiie: 523k ohatae tdi Me Man eb inltyy oSle Tuer cetng eet shatae At 15
Vientre inmaculado (sin manchas blancas)............ Epipedobates machalilla
Vientrecon-manchas Dlaneas: sta ssacedacdsSapcsnd tres pees ane cote ancph nantiodas aatodeace at 16
Membrana extensa entre los dedos de los pies........... Hyloxalus elachyhistus
Membrana limitada entre los dedos .0..... eee eee Ayloxalus infraguttatus
Vientre transparente con el peritoneo blanco y los pulmones visibles, superfi-
cies dorsales verdes con manchas amarillas....... Hyalinobatrachium tatayoi
Vientre no transparente y érganos internos no visibles, superficies dorsales
IAL HONS OPIS OU CLOG ta teensoneacenisnaae dea shelenenmee ne inedimmmecenctntscuaelinninibenioveinds 18
Dedos de la mano sin membranas interdigitales ....... else eseeeeeeereeeees 19
Membranas interdigitales presentes entre los dedos de la mano................ 26

Dedo III del pie mas largo que el Dedo V; puntas de los dedos solo ligera-

mente expandidas (hinchadas); glandulas blancas bien definidas posteriores al

AUG 2S LAr TANG F as poh Pare desn base Rann oder la ddan Medien son gl Barycholos pulcher
DéedoVadelpicinasilarco tue cD edo Me castes ceites sesh ibid cbmesett 20
Dedos del pie que carecen de membranas extemsas.........sceeeeseeseeeeeeeneeeeees 21
Membranas interdigitales presentes entre los dedos de los pies ............004+ 24
Dedo I del mano mas largo que el Dedo II; pliegues dorsolaterales presentes
eel sgises co acta Pace stes as oats Pac ues si alesdes vio ales seine Mews es se Hoaev eve ecnnie gnc h to's gg geo cey giteest one 22

36

22

Diego Armijos-Ojeda et al. / ZooKeys 1063: 23—48 (2021)

Discos en los dedos relativamente pequefios; superficie interna del tarso con
pliegue largo; superficies posteriores de los muslos negras con manchas 0 re-
ticulaciones blancas; LHC de adultos 25-73 mm......... Pristimantis lymani
Discos en los dedos anchos; tubérculo tarsal interno pequefio; superficies pos-
teriores de los muslos marrones con pequefias manchas color crema; LHC de
ACEO SED S= AG rain ey ee eee eae Lee _e emer ee Pristimantis achatinus
Hocico con papila en la punta; talon con pequefio tubérculo cénico; LHC de
ACCC SOLS SATIN. aia Bc cyesiessee de Seatase dee cdSeerios Pristimantis subsigillatus
Hocico sin papila en la punta; talén sin tubérculos; ingle negra con manchas
amarillas;- LAC de-adultos?l 3=2 5: mints is350-esescedretcanes Pristimantis walkeri
Mandibula inferior con una hilera de tubérculos; hocico largo; moteado ne-
gro y azul en la ingle y en las superficies anterior y posterior de los muslos....
se eee at Deets atic ae ee eget eee eee Scinax sugillatus

Huesos de las patas visibles a través de la piel, de color blanco a blanco azu-
lado; dorso con pequefios tubérculos, dispersos a abundantes ............ eee
Las athena nena ftw ace tenena Soak setae Rehepaaittsegss Bohs Re Shes cee Scinax quinquefasciatus
Huesos de las patas visibles a través de la piel, verdes; dorso sin tubérculos....
BARR AS oe tp MEARE el, ey LRA SI A Scinax tsachila
Parte superior de la cabeza co-osificada y rugosa (craneo co-osificado tegu-
mentario-craneal); iris dorado con manchas negras irregulares; LHC de adul-
COS OHM erty 5 ro Hest, Pe ceases ates haan toeen seed? Trachycephalus jordani
Parte:superior de’ latcabezaimo.co-osilicada 4; 223010. bese.tve contend eazt tng ebpedabeeetee es 27.
Piel en el dorso tuberculada; membrana extensa entre los dedos de la mano;
coloracioén dorsal generalmente marr6n....... eee eects Boana rosenbergi
Piel lisa en el dorso; membrana entre los dedos basal a moderada.............. 28
Calcar pronunciado en el tal6n; membrana entre los dedos de la mano mod-
erada; coloracién dorsal generalmente verde; iris amarillento ....0... eee
leat eiUhs ets i aaa. ie soi en an Se mae Eases eas Ray teenie oacdes Boana pellucens

Membrana entre los dedos de la mano moderada; iris dorado con manchas
negras irregulares; piel glandular gruesa en la cabeza y dorso..... esses eeeeees
Be PRR oie iro Oe oe Orci Arka re Be Rha te OR Trachycephalus quadrangulum
Membrana entre los dedos de la mano basal; marca postorbital oscura carac-
teristicastranja-la bial blanca. e.cseroncsiete evercosesteceveesnteeneee Smilisca phaeota

Discussion

We provide the first comprehensive amphibian species checklist for the Equatorial SDE

including 30 species. In addition to compiling the available data from published sources,
museum collections and online databases, we contribute a large amount of original in-

formation generated through extensive field surveys (two thirds of all reported informa-

Amphibians of the equatorial seasonally dry forest DF

ae
Rhinella__|
nortbtis|

4,
Pe

Jige 0 50 100 km
aS

= | =f us ~ Hyloxalus”
y i infragu

Figure 3. Distribution records of Bufonidae, Centrolenidae, Ceratophryidae and Dendrobatidae in
the Equatorial Seasonally Dry Forest (SDF). Maps are given for the families Bufonidae (R/inella alata,
R. horribilis), Centrolenidae (Hyalinobatrachium tatayoi), Ceratophryidae (Ceratophrys stolemanni) and
Dendrobatidae (Epipedobates anthonyi, E. machalilla, Hyloxalus elachyhistus, H. infraguttatus). For Cera-
tophrys stolzmanni, blue points represent new distributional records for the species, the two southernmost

localities and the highest altitude, respectively.

tion for the area). Although the records reported here significantly add to our previous
understanding of tropical amphibian communities in South American seasonally dry
habitats, the dataset probably underestimates the actual amphibian diversity in the area.

Although the Equatorial SDF has been overall understudied, the lack of informa-
tion is most evident in the Peruvian part of this ecoregion. For a better understanding,
further efforts to disseminate currently unpublished amphibian distribution records of
Peruvian researchers and taxonomically clarify the identity of amphibians which are
currently assigned only at genus level (e.g., Venegas 2005) are necessary. From the total
dataset, less than 4% of the records were from Peru, although 63.5% of Equatorial SDF
area corresponds to this country. A lower amphibian richness is expected in certain Pe-
ruvian regions, such as the area bordering the Sechuran desert, due to the hostile envi-
ronmental conditions. The bibliographic search and a comparison with similar habitats
in Ecuador suggest that the lack of data regarding amphibian diversity in the Peruvian
part of the Equatorial SDF is due to sampling bias rather than accurately reflecting
the absence of this taxa. Even in Ecuador, where sampling was carried out more ho-
mogenously throughout the study area, there is still a shortage of adequate amphibian

38 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23—48 (2021)

73°w

ee
se

= Be oar a -| 4 Sa eae.
Engystomops | ; Engystomops ' Engystomo} 5
guayaco |_ i Mm pustulatus |_ puyango |

ue
Ecuador od Ecuador

Sd

Tey a ae 5 y are =
Leptodactylu: Leptodactylus “Leptodactylus
(oo ti | fa

melanonott ventrimaculatus

Ecuador | én Ecuador

Figure 4. Distribution records for the Leptodactylidae family in the Equatorial Seasonally Dry Forest
(SDF). In blue, distribution range extensions: for Engystomops puyango, the northernmost locality is more

than 70 km from the previously known distribution; for E. randi, the first record in Peru.

inventories, especially outside protected areas (Ortega-Andrade et al. 2021). Further ef-
forts to inventory the extensive underexplored areas to correctly evaluate the amphibian
community status should constitute a priority (Ortega-Andrade et al. 2021).

The fact that, out of the 30 species present in the Equatorial SDF, five have been
described as new for science in the last 20 years (Scinax tsachila, Engystomops guayaco,
E. montubio, E. puyango, E. randi) further emphasizes the need for intense and focused
research targeted at undersampled locations. The list of amphibians present in the
Equatorial SDF can change in the future because of updated taxonomic studies based
on modern integrative techniques that use morphological, molecular, and behavioral
data. It is the case of the cane toads (R. Aorribilis), for which a recent study indicates
that the species present in these forests might be phylogenetically distinct from the
rest of the range (Pereyra et al. 2021). Similarly, a species of milk frog (Trachycephalus
quadrangulum) was resurrected after being included in the 7’ typhonius species complex
for 50 years, as was the toad Rhinella alata, after being synonymized to R. margaritifera.
It is likely that a similar fate awaits species in the genera Pristimantis, Leptodactylus and
Hyloxalus, for which taxonomical delimitation is currently based on morphological
characters only, allowing for the existence of cryptic taxa.

We include the information on important life history characteristics for all am-
phibian species present in the Equatorial SDE It is recommended that prioritization of

Amphibians of the equatorial seasonally dry forest 3°

Boana 5 Scinax
rosenbergi | y quinquefasciatus|

Scinal ;
ae

Ecuador

L
Sot

7]

-

=

eee

Se 0 50) 100 km
a

eS

Sane Few ——
Trachycephalus lus
quadrangulu 1

n
Sof

slew

Figure 5. Distribution records for the Hylidae family in the Equatorial Seasonally Dry Forest (SDF). In
blue, the first report of Trachycephalus quadrangulum in Loja province.

conservation measures should consider functional diversity of an assemblage, not only
species richness, since species make differential contribution to the functioning of their
ecosystem (Campos et al. 2017; Bolochio et al. 2020). Currently, research conducted
on life-history is scarce for most of the 30 amphibian species. As more information
becomes available, the inclusion of additional traits, might offer a more complete im-
age of the native amphibian communities and their capacity to withstand landscape
changes. The current insufficient knowledge regarding Equatorial SDF species threats
and risks, in addition to the fact that some have been only recently (re)described, re-
sults in the five species that are lacking a global conservation status assessment.

Seven of the 30 species (23.3%) have a distribution exclusively or almost-exclusive-
ly restricted to the Equatorial SDE. Although amphibian species living in tropical dry
forests are inherently more tolerant to high temperatures and desiccation, they are still
expected to be vulnerable to the predicted climate changes because they are already ex-
posed to conditions at the limit of their physiological tolerance (Catenazzi et al. 2014;
Székely et al. 2018). No studies modelling the sensitivity to climate change scenarios
have been carried out for the species endemic to the Equatorial SDF. Some of the spe-
cies have adapted to anthropized environments, and in some cases their distribution
extends to other ecosystems adjacent to the dry forest. However, the small extent and
fragmented limits of the Equatorial SDF, coupled with the land-use change that affects
this ecoregion, represent a risk that, in the case of climate change, these species face a re-

40 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

Pristimantis
subsigillatus’

Figure 6. Distribution records of Ranidae and Craugastoridae in the Equatorial Seasonally Dry Forest
(SDF). Maps are given for Ranidae (Lithobates bwana) and Craugastoridae (Barycholos pulcher, Pristiman-
tis achatinus, P lymani, P subsigillatus, and P walkeri).

duction of suitable habitat (Nowakowski et al. 2017), even if currently they also occur
in protected areas. This emphasizes the need for the species with a narrow distribution
to be targeted for urgent monitoring and conservation measures (Sodhi et al 2008).

Conservation aspects

The current loss of biodiversity in the study area is the synergic result of a multitude
of factors, the most important being habitat loss, fragmentation, pollution, intro-
duction of alien species and unsustainable use of resources (Ceballos and Ortega-
Baes 2011). The Equatorial SDF is under severe anthropic pressure (Jara-Guerrero
et al. 2019), experiencing a dramatic loss in area in the quality of these forests,
exacerbating the biodiversity losses that occurred during the last century, mainly
because of agricultural and urban expansion (Mittermeier et al. 1999; Sierra 2013).
Originally, 35% of coastal Ecuador was naturally covered with Equatorial SDF,
but this ecosystem was reduced to less than 2% by the 1990s (Dodson and Gentry
1991). This alarming situation has catalyzed an effort to protect the last remnants
and isolated patches of tropical dry forest (Gentry 1977; Parker and Carr 1992; Best
and Kessler 1995; Espinosa et al. 2012; Sierra 2013; Tapia-Armijos et al. 2015).
Estimated yearly rate of deforestation in the area was on average of 1.6% between

Amphibians of the equatorial seasonally dry forest 4]

2000 and 2010 (Sierra 2013). Making matters worse is the fact that the remnants
are highly fragmented, reducing their potential of regeneration (Tapia-Armijos et
al. 2015). In this context, there is an urgent need for future research evaluating the
efficiency of protected areas for the conservation of Equatorial SDF amphibians,
under different scenarios of global change.

The level of protection for Equatorial SDF is extremely low (Rivas et al. 2020), less
than 5% of its territory being included in nationally protected areas in Ecuador and
Peru (Escribano-Avila et al. 2017). To alleviate this aspect, several private entities and
local communities are taking steps forward to protect key areas in the region (Escriba-
no-Avila et al. 2017). However, the conservation of this and other ecosystems cannot
and should not be the exclusive responsibility of NGOs. The governments of Ecuador
and Peru, the civil society of each country (including universities and research centers),
and the international community must become more involved in these processes. An
essential part of this support is providing the correct information and analysis regard-
ing species distribution, ecology, and status of conservation.

Acknowledgements

Research permits were issued by Ministerio del Ambiente, Agua y Transicién Ecoldgi-
ca del Ecuador: MAE-DNB-CM-2015-0016, granted to Universidad Técnica Par-
ticular de Loja; MAAE-ARSFC-2020-0727 granted to Paul Székely; MAAE-ARS-
FC-2020-0960, granted to Diego Armijos-Ojeda; 009-IC-FAN-DPEO-MAE, grant-
ed to Diego EF. Cisneros-Heredia, Universidad San Francisco de Quito.

Fieldwork was partially funded by The Rufford Foundation (grant no. 30020-1 “Pro-
tecting the tropical dry forest, home to unique amphibians”).

DFCH’s work was possible thanks to financial support granted to different research
projects by Gobierno Auténomo Descentralizado Provincial de El Oro GADPEO, Uni-
versidad San Francisco de Quito USFQ, Fundacién Natura, Bidésfera Gesti6n Ambiental,
Sun Conservation S.A., and Secretaria de Educacion Superior, Ciencia, Tecnologia e In-
novacién SENESCYT (Programa Becas de Excelencia).

We are grateful to Claudia Koch and Matthew Metcalf for their constructive com-
ments that helped to improve our manuscript.

We thank all the persons who, through their contribution in terms of logistics and
lodgings, have helped us during fieldwork at various sites: rangers in Reserva Ecologica
Arenillas, Sandro Trigrero (Comunidad Dos Mangas), Silvano Quimiz (Comunidad Rio
Blanco), Mariela Loor (Reserva Lalo Loor), Belarmino Camacho and his wife (Manga-
hurco), Felipe Sanchez and Elsita Castillo (Cabeza de Toro), Guilbert Olaya, Mayely
Aponte and Mrs. Astrid (Cazaderos), Mikaela Soto and her husband (Hotel Los Guaya-
canes), Darwin Martinez (NCI Zapotillo), park rangers and officers of the Ministerio del
Ambiente in Puyango, Italo Encalada (Bosque Petrificado de Puyango), park rangers and
officers of the Ministerio del Ambiente in Machalilla, Carlos Zambrano, Andrés Baquero,
Diego Mosquera, Galo Echeverria (Parque Nacional Machalilla). We are grateful to the

42 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

persons who have contributed their field data: Mario Yanez, Fausto Siavichay, Patricia Be-
jarano, Daniela Sanchez, Juan Carlos Sanchez, and Luis Oyagata. Special thanks to Judit
Vorés, Maria Fernanda Burneo, Ana Paula Cabrera, and Pamela Aponte, for their help
during fieldwork, and Ivonne Gonzalez for her support with the spatial analyses process.

DFCH thanks Maria Elena Heredia, Laura Heredia, Jonathan Guillemot, Nicole
Acosta, Mateo Davila, Emilia Pefaherrera, Alejandro Montalvo, Diego Mosquera, An-
drés Baquero, Galo Echeverria, Italo Encalada, Pablo Beltran, Daniela Proafo, Karina
Dammer, Kelly Swing, Jean-Marc Touzet, and Francisco Vintimilla for their valuable

support during fieldwork and lab work.

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Supplementary material |

Tables S1, S2

Authors: Diego Armijos-Ojeda, Diana Székely, Paul Székely, Dan Cogalniceanu,

Diego EF Cisneros-Heredia, Leonardo Ordéfez-Delgado, Adrian Escudero,

Carlos Ivan Espinosa

Data type: species data

Explanation note: List of ecosystem types included in the Equatorial Seasonally Dry Forest,
based on MAE 2013 and MINAM 2019. Presence of amphibian species in the provinc-
es (Ecuador) or departments (Peru) throughout the Equatorial Seasonally Dry Forest.

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.

Link: https://doi.org/10.3897/zookeys. 1063.69580.suppl1

48 Diego Armijos-Ojeda et al. / ZooKeys 1063: 23-48 (2021)

Supplementary material 2

Appendix 1. Reference list for life-history characteristics of amphibians of the

Equatorial Seasonally Dry Forest (Table 1)

Authors: Diego Armijos-Ojeda, Diana Székely, Paul Székely, Dan Cogalniceanu,

Diego EF. Cisneros-Heredia, Leonardo Orddéfez-Delgado, Adrian Escudero,

Carlos Ivan Espinosa

Data type: reference list

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.

Link: https://doi.org/10.3897/zookeys. 1063.69580.suppl2

Supplementary material 3

Dataset including amphibian species occurence information, museum specimen

numbers, source of data

Authors: Diego Armijos-Ojeda, Diana Székely, Paul Székely, Dan Cogalniceanu,

Diego FE. Cisneros-Heredia, Leonardo Orddéfez-Delgado, Adrian Escudero,

Carlos Ivan Espinosa

Data type: species data

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.

Link: https://doi.org/10.3897/zookeys. 1063.69580.suppl3