Seasonally dry forests (SDFs) are one of the most challenging ecosystems for amphibians, fueling the diversity 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 SDF, 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 under-sampled areas, using modern taxonomic methods. The study emphasizes the conservation priorities in the Equatorial SDF, based on the distribution, conservation status and life-history data. This information should be useful for the local authorities and institutions involved in the management and conservation of biodiversity in SDF.

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

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 (Sánchez‐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 allowing 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 Ecuadorian-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 Marañon, 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 SDF, 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, consequently, a global priority for conservation (DryFlor 2016) and a hotspot for biodiversity (Myers et al. 2000). Other authors have referred to this area under different (complete or partially synonym) names: Ecuadorian Subcentre (Müller 1973), Guayas Province (Ringuelet 1975), Ecuadorian Pacific Dry Forest (Udvardy 1975), Pacific Equatorial Dominion (Ab’Saber 1977), Tumbesian Centre (Cracraft 1985), Ecuadorian Dry Forest and Western Ecuador Moist Forest (Dinnerstein 1995), Western Ecuador Province (Morrone 1999), Arid Ecuadorian and Túmbes-Piura Provinces (Morrone 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 (Almendáriz and Carr 1992, 2012; Venegas 2005; Cisneros-Heredia 2006; Armijos-Ojeda and Valarezo 2010; Amador and Martínez 2011; Székely et al. 2016; Sánchez-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 distribution 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 prioritize conservation actions, promote public awareness and focus further inventory efforts towards areas where gaps remain.

The final dataset consists of 2,032 distribution records spread throughout the Equatorial 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 iNaturalist contributed 286 data points, representing 14.1% of the dataset (Fig. 1 – Database).

Overall, we report 30 amphibian species for the Equatorial SDF, belonging to 14 genera and eight families (Figs 2–6); 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 stolzmanni, 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 SDF, with few occurrences in adjacent habitats, characterized by higher humidity/altitude. The remaining 23 species have a wider distribution.

Figure 2. 

Amphibian species of the Equatorial Seasonally Dry Forest A Rhinella alata (photo by Silvia Aldás, https://bioweb.bio) B Rhinella horribilis C Hyalinobatrachium tatayoi D Ceratophrys stolzmanni E Epipedobates anthonyi F Epipedobates machalilla G Hyloxalus elachyhistus H Hyloxalus infraguttatus I 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 quadrangulum Q Engystomops guayaco R Engystomops montubio S Engystomops pustulatus T Engystomops puyango U Engystomops randi V Leptodactylus labrosus W Leptodactylus melanonotus X Leptodactylus ventrimaculatus Y Barycholos pulcher Z Pristimantis achatinus AA Pristimantis lymani AB Pristimantis subsigillatus AC Pristimantis walkeri (photograph by Santiago R. Ron, https://bioweb.bio) AD Lithobates bwana. Habitat seasonal change (Reserva Ecológica Arenillas) AE april (rainy season) AF december (dry season).

Regarding the global extinction risk status (IUCN 2021), one (C. stolzmanni) is classified as Vulnerable, and three are Near Threatened (E. anthonyi, Hyalinobatrachium tatayoi, and Hyloxalus infraguttatus). Two are Data Deficient (Rhinella alata and Engystomops guayaco) and another three (R. horribilis, Scinax tsachila and Trachycephalus quadrangulum) are currently Not Evaluated, while the remaining 21 species have a Least Concern IUCN status (Table 1).

Changes in distribution range

We report here the extension of the distribution ranges of four amphibian species detected during fieldwork.

Ceratophrys stolzmanni (Pacific horned frog). This species is endemic to the lowland 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 (Manabí, Ecuador), in the north. Distribution follows the Pacific coast, the innermost point being 50 km from the coast (Cuadrado et al. 2020), but all previously recorded locations were at low altitudes (up to 130 m a.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 Manabí, 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 Cazaderos (4.0259°S, 80.4497°W, 221 m a.s.l.) and Mangahurco, Área de Conservación Municipal Los Guayacanes (4.1611°S, 80.4388°W, 360 m a.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.

Figure 3. 

Distribution records of Bufonidae, Centrolenidae, Ceratophryidae and Dendrobatidae in the Equatorial Seasonally Dry Forest (SDF). Maps are given for the families Bufonidae (Rhinella alata, R. horribilis), Centrolenidae (Hyalinobatrachium tatayoi), Ceratophryidae (Ceratophrys stolzmanni) and Dendrobatidae (Epipedobates anthonyi, E. machalilla, Hyloxalus elachyhistus, H. infraguttatus). For Ceratophrys stolzmanni, blue points represent new distributional records for the species, the two southernmost localities and the highest altitude, respectively.

Engystomops puyango (Puyango dwarf frog). This small amphibian was recently described 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 m a.s.l.), El Oro province, more than 72 km from the type locality, constitutes the farthest record from the known distribution (Fig. 4).

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.

Engystomops randi (Rand’s dwarf frog). Another recently described leptodactylid species, which has a wider distribution, encompassing most of the Equatorial SDF 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 contribute a new locality for Loja province in Ecuador, close to Bolaspamba (4.1823°S, 80.3692°W, 416 m a.s.l.) (Fig. 5).

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.

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, Pristimantis achatinus, P. lymani, P. subsigillatus, and P. walkeri).

We provide the first comprehensive amphibian species checklist for the Equatorial SDF, 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 information generated through extensive field surveys (two thirds of all reported information 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 information 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 Peruvian regions, such as the area bordering the Sechuran desert, due to the hostile environmental 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 homogenously throughout the study area, there is still a shortage of adequate amphibian inventories, especially outside protected areas (Ortega-Andrade et al. 2021). Further efforts 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. horribilis), 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 T. 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 amphibian species present in the Equatorial SDF. It is recommended that prioritization of 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 image 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, results 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-exclusively restricted to the Equatorial SDF. 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 exposed 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 species 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 reduction 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).

Research permits were issued by Ministerio del Ambiente, Agua y Transición Ecológica del Ecuador: MAE-DNB-CM-2015-0016, granted to Universidad Técnica Particular de Loja; MAAE-ARSFC-2020-0727 granted to Paul Székely; MAAE-ARSFC-2020-0960, granted to Diego Armijos-Ojeda; 009-IC-FAN-DPEO-MAE, granted to Diego F. Cisneros-Heredia, Universidad San Francisco de Quito.

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

DFCH’s work was possible thanks to financial support granted to different research projects by Gobierno Autónomo Descentralizado Provincial de El Oro GADPEO, Universidad San Francisco de Quito USFQ, Fundación Natura, Biósfera Gestión Ambiental, Sun Conservation S.A., and Secretaría de Educación Superior, Ciencia, Tecnología e Innovación SENESCYT (Programa Becas de Excelencia).

We are grateful to Claudia Koch and Matthew Metcalf for their constructive comments 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 (Mangahurco), Felipe Sánchez and Elsita Castillo (Cabeza de Toro), Guilbert Olaya, Mayely Aponte and Mrs. Astrid (Cazaderos), Mikaela Soto and her husband (Hotel Los Guayacanes), Darwin Martínez (NCI Zapotillo), park rangers and officers of the Ministerio del Ambiente in Puyango, Ítalo Encalada (Bosque Petrificado de Puyango), park rangers and officers of the Ministerio del Ambiente in Machalilla, Carlos Zambrano, Andrés Baquero, Diego Mosquera, Galo Echeverría (Parque Nacional Machalilla). We are grateful to the persons who have contributed their field data: Mario Yánez, Fausto Siavichay, Patricia Bejarano, Daniela Sánchez, Juan Carlos Sánchez, and Luis Oyagata. Special thanks to Judit Vörös, María Fernanda Burneo, Ana Paula Cabrera, and Pamela Aponte, for their help during fieldwork, and Ivonne González for her support with the spatial analyses process.

DFCH thanks María Elena Heredia, Laura Heredia, Jonathan Guillemot, Nicole Acosta, Mateo Dávila, Emilia Peñaherrera, Alejandro Montalvo, Diego Mosquera, Andrés Baquero, Galo Echeverría, Italo Encalada, Pablo Beltrán, Daniela Proaño, Karina Dammer, Kelly Swing, Jean-Marc Touzet, and Francisco Vintimilla for their valuable support during fieldwork and lab work.