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Divergence of tropical pitvipers promoted by independent colonization events of dry montane Andean habitats

2019 , Salazar Valenzuela, David , Kuch U. , Torres-Carvajal O. , Valencia J.H. , Gibbs H.L.

Aim: A poorly explored feature of the origin and maintenance of Neotropical biodiversity is how the evolutionary dynamics of colonization and differentiation in relation to lowland and highland habitats has impacted lineage formation. Most speciation models for this region have focused on vicariant events, whereas the need to assess the influence of demographic processes has been recognized only recently. We evaluate if the origin of Andean montane lineages of terciopelo pitvipers is explained by either of two historical processes that represent distinct phylogeographic mechanisms: differentiation by isolation within the highlands or different dispersal events from the lowlands. Location: Western Ecuador. Taxon: Terciopelo pitvipers (Bothrops asper species complex). Methods: We use genomic data and genetic clustering analyses, evaluation of historical migration between genetic clusters and demographic model selection to investigate recent diversification events in South America using a vertebrate group rarely explored in phylogeographic studies: tropical Andean snakes. Specifically, the origin of two Ecuadorian montane lineages of terciopelo pitvipers was evaluated given ambiguous phylogenetic relationships with the presumably ancestral Pacific lowland lineage. Results: Discrepancies of evolutionary relationships previously obtained with tree-like methods are resolved through the use of modelling approaches. We found strong support for the independent origin of montane lineages based on topologies inferred by maximum-likelihood trees and modelling approaches that take into account possible gene flow. This suggests dispersal rather than in-situ differentiation as the most likely mechanism by which the montane linages originated. Main conclusions: Recent large-scale studies have found support for identifying dispersal events as important drivers of diversification in the Neotropical region. We contribute to these ideas by identifying a fine-scale case in a rarely studied group of animals -Andean snakes- in which river valleys acted as an entrance for the upward colonization of montane dry habitats and subsequent ecological diversification. © 2019 John Wiley & Sons Ltd

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A roadmap for harlequin frog systematics, with a partial revision of Amazonian species related to Atelopus spumarius

2025 , STEFAN LÖTTERS , PHILIPP BÖNING , SALVADOR BAILON , JOSE DANIEL BARROS CASTAÑEDA , RENAUD BOISTEL , ALESSANDRO CATENAZZI , JUAN C. CHAPARRO , GERMÁN CHÁVEZ , ANGEL CHUJUTALLI , LAURENT COEN , LUIS A. COLOMA , ANDREW J. CRAWFORD , JAIME CULEBRAS , JUAN CARLOS CUSI MARTÍNEZ , JUAN MANUEL DAZA , IGNACIO DE LA RIVA , DENISE J. ELLWEIN , RAFFAEL ERNST , SANDRA V. FLECHAS , ANTOINE FOUQUET , JUAN MANUEL GUAYASAMIN , CHRISTOPHER HEINE , RAFAEL F. JORGE , ALISHA JUNG , KARL-HEINZ JUNGFER , NATHALIE KAFFENBERGER , HENRIK KREHENWINKEL , ENRIQUE LA MARCA , MARGARITA LAMPO , GUIDO F. MEDINA RANGEL , LUDVIG ORSEN , DANIEL J. PALUH , JOSÉ LUIS PÉREZ GONZALEZ , JONATHAN PERRIN , AMANDA B. QUEZADA RIERA , JUAN PABLO REYES-PUIG , BERNARDO ROCA-REY ROSS , DANIELA C. RÖSSLER , LUIS ALBERTO RUEDA SOLANO , Salazar Valenzuela, David , JOSEFA CELSA SEÑARIS VAZQUEZ , MORGANE SOWINSKI , ANDREA TERÁN-VALDEZ , ANGIE TOVAR-ORTIZ , MICHAEL VEITH , PABLO VENEGAS , RUDOLF VON MAY , TIMM WEITKAMP , AMADEUS PLEWNIA

Harlequin frogs, genus Atelopus, are a species-rich group of bufonid anurans from the Neotropics with more than 100 species. For nearly four decades now, this group has suffered from massive population declines. Almost all species are threatened with extinction, and many populations and several species are considered extinct or possibly extinct. This results in a limited sampling available for studies on harlequin frog systematics, especially in terms of molecular genetic information. However, efficient conservation of harlequin frogs requires an improved taxonomy. This is further complicated through the circumstance that many Atelopus species are relatively poor in external morphological characters combined with a high level of intra-specific character variation (e.g. coloration and body size). At the same time, cryptic diversity exists with well differentiated species (supported by osteology and molecular genetics) almost indistinguishable by external morphology. We compiled the largest dataset to date for mitochondrial (12S, 16S, cyt b) and nuclear (POMC, RAG1) markers and present a phylogeny (likelihood and Bayesian inference methods) including 152 samples from 104 populations scattered over the entire geographic range of the genus. Four allo- or parapatric main clades are distinguished: I. Sierra Nevada; II. Venezuelan-Andean; III. Andean-Chocó-Central American (with the ignescens and the varius-longirostris clades); and IV Amazonian (containing the tricolor and the flavescens-spumarius clades). The phylogenetic relationships within these clades remain to be resolved. Taxonomic implications included both splitting and lumping, but taxonomic action is here only taken for populations related to A. spumarius from western Amazonia. Besides redescriptions of A. spumarius sensu stricto and A. colomai, we describe two new species based on morphology, skull osteology and bioacoustics. Additional yet understudied populations from Amazonia may be allocated to these species or may represent additional undescribed taxa.

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Feeding ecology of the Terciopelo pit viper snake (Bothrops asper) in Ecuador

2023 , Loaiza-Lange A. , Székely D , Torres-Carvajal O. , Tinoco N. , Salazar Valenzuela, David , Székely P.

Thoroughly documenting prey items and diet composition is crucial for understanding a predator’s role in the ecosystem. In gape restricted predators, such as snakes, documenting and analyzing the type and size of the prey is important to interpret their ecological role. We describe the diet patterns of a species of venomous snake, the Terciopelo pit viper (Bothrops asper), from its Ecuadorian populations. Examining the gastrointestinal contents of museum specimens collected over an extensive area of the Pacific lowlands of Ecuador, we encountered 69 identifiable prey items from four major taxonomic groups (amphibians, centipedes, mammals, and reptiles). We evaluated the observed composition of prey to check for differences between sexes and size-classes. To complement our observations of the Terciopelo species complex throughout their distribution, we carried out a systematic literature review. Our data show an ontogenetic shift in diet, with a transition from more diverse diet in juveniles towards a mammal-specialized diet in adults, and distinct proportion of prey taxa between the sexes in the juvenile size class. Copyright 2023 Loaiza-Lange et al.

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A new species of pitviper of the genus Bothrops (Serpentes: Viperidae: Crotalinae) from the Central Andes of South America

2019 , Timms J. , Chaparro J.C. , Venegas P.J. , Salazar Valenzuela, David , Scrocchi G. , Cuevas J. , Leynaud G. , Carrasco P.A.

We describe a new species of montane pitviper of the genus Bothrops from the Cordillera Oriental of the Central Andes, distributed from southern Peru to central Bolivia. The new species can be distinguished from its congeners by the characteristic combination of a dorsal body color pattern consisting of triangular or subtriangular dark brown dorsal blotches, paired dark brown parallel occipital stripes, a conspicuous dark brown postocular stripe, the presence of canthorostrals in some specimens, prelacunal fused or partially fused with second supralabial, one scale usually separating internasals, rostral trapezoidal, two canthals oval to rounded, similar size or slightly larger than internasals, three or four medial intercanthals, eight to twelve intersupraoculars, intercanthals and intersupraoculars keeled and frequently slightly keeled, supraoculars oval, one to three suboculars, two to three postoculars, loreal subtriangular, two to six prefoveals, subfoveals absent, two or none postfoveals, one or two scales between suboculars and fourth supralabial, seven or eight supralabials, nine or eleven infralabials, 23-25 middorsal scales, 189-195 ventrals in females and 182-190 in males, 48-58 subcaudals in females and 54-63 in males, exceptionally undivided. The new species is apparently restricted to areas within Andean montane forests that are less humid and devoid of large trees. Copyright © 2019 Magnolia Press.

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Path for recovery: an ecological overview of the Jambato Harlequin Toad (Bufonidae: Atelopus ignescens) in its last known locality, Angamarca Valley, Ecuador

2024 , Mateo A. Vega-Yánez , Amanda B. Quezada-Riera , Blanca Rios-Touma , María del Carmen Vizcaíno-Barba , William Millingalli , Orlando Ganzino , Luis A. Coloma , Elicio E. Tapia , Nadine Dupérré , Mónica Páez-Vacas , David Parra-Puente , Daniela Franco-Mena , Gabriela Gavilanes , Salazar Valenzuela, David , Carlos A. Valle , Juan M. Guayasamin

The Jambato Harlequin toad (Atelopus ignescens), a formerly abundant species in the Andes of Ecuador, faced a dramatic population decline in the 1980s, with its last recorded sighting in 1988. The species was considered Extinct by the IUCN until 2016, when a fortuitous discovery of one Jambato by a local boy reignited hope. In this study, we present findings from an investigation conducted in the Angamarca parish, focusing on distribution, abundance, habitat preferences, ecology, disease susceptibility, and dietary habits of the species. In one year we identified 71 individuals at different stages of development in various habitats, with a significant presence in agricultural mosaic areas and locations near water sources used for crop irrigation, demonstrating the persistence of the species in a complex landscape, with considerable human intervention. The dietary analysis based on fecal samples indicated a diverse prey selection, primarily comprising arthropods such as Acari, Coleoptera, and ants. Amphibian declines have been associated with diseases and climate change; notably, our study confirmed the presence of the pathogen Batrachochytrium dendrobatidis (Bd), but, surprisingly, none of the infected Jambatos displayed visible signs of illness. When analyzing climatic patterns, we found that there are climatic differences between historical localities and Angamarca; the temporal analysis also exposes a generalized warming trend. Finally, in collaboration with the local community, we developed a series of management recommendations for terrestrial and aquatic environments occupied by the Jambato.

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Why Do Some Lineages Radiate While Others Do Not? Perspectives for Future Research on Adaptive Radiations

2025 , Rishi De-Kayne , Rowan Schley , Julia M.I. Barth , Luke C. Campillo , Catalina Chaparro-Pedraza , Jahnavi Joshi , Walter Salzburger , Bert Van Bocxlaer , Darko D. Cotoras , Carmelo Fruciano , Anthony J. Geneva , Rosemary Gillespie , Joseph Heras , Stephan Koblmüller , Blake Matthews , Renske E. Onstein , Ole Seehausen , Pooja Singh , Erik I. Svensson , Salazar Valenzuela, David , Maarten P.M. Vanhove , Guinevere O.U. Wogan , Ryo Yamaguchi , Anne D. Yoder , José Cerca

Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation. This record is sourced from MEDLINE/PubMed, a database of the U.S. National Library of Medicine

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Evaluating the utility of camera traps in field studies of predation

2019 , Akcali C.K. , Pérez-Mendoza H.A. , Salazar Valenzuela, David , Kikuchi D.W. , Guayasamin, Juan M. , Pfennig D.W.

Artificial prey techniques-wherein synthetic replicas of real organisms are placed in natural habitats-are widely used to study predation in the field.We investigated the extent to which videography could provide additional information to such studies. As a part of studies on aposematism and mimicry of coral snakes (Micrurus) and their mimics, observational data from 109 artificial snake prey were collected from video-recording camera traps in three locations in the Americas (terra firme forest, Tiputini Biodiversity Station, Ecuador; premontane wet forest, Nahá Reserve, Mexico; longleaf pine forest, Southeastern Coastal Plain, North Carolina, USA). During 1,536 camera days, a total of 268 observations of 20 putative snake predator species were recorded in the vicinity of artificial prey. Predators were observed to detect artificial prey 52 times, but only 21 attacks were recorded. Mammals were the most commonly recorded group of predators near replicas (243) and were responsible for most detections (48) and attacks (20). There was no difference between avian or mammalian predators in their probability of detecting replicas nor in their probability of attacking replicas after detecting them. Bite and beak marks left on clay replicas registered a higher ratio of avian:mammalian attacks than videos registered. Approximately 61.5% of artificial prey monitored with cameras remained undetected by predators throughout the duration of the experiments. Observational data collected from videos could provide more robust inferences on the relative fitness of different prey phenotypes, predator behavior, and the relative contribution of different predator species to selection on prey. However, we estimate that the level of predator activity necessary for the benefit of additional information that videos provide to be worth their financial costs is achieved in fewer than 20% of published artificial prey studies. Although we suggest future predation studies employing artificial prey to consider using videography as a tool to inspire new, more focused inquiry, the investment in camera traps is unlikely to be worth the expense for most artificial prey studies until the cost:benefit ratio decreases. © 2019 PeerJ Inc. All rights reserved.

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Bothrops atrox from Ecuadorian Amazon: Initial analyses of venoms from individuals

2021 , Patiño R.S.P. , Salazar Valenzuela, David , Medina-Villamizar E. , Mendes B. , Proaño-Bolaños C. , da Silva S.L. , Almeida J.R.

Bothrops atrox is the most clinically relevant snake species within the Amazon region, which includes Ecuadorian territories. It comprises a large distribution, which could contribute to the genetic and venomic variation identified in the species. The high variability and protein isoform diversity of its venom are of medical interest, since it can influence the clinical manifestations caused by envenomation and its treatment. However, in Ecuador there is insufficient information on the diversity of venomic phenotypes, even of relevant species such as B. atrox. Here, we characterized the biochemical and toxicological profiles of the venom of six B. atrox individuals from the Ecuadorian Amazon. Differences in catalytic activities of toxins, elution profiles in liquid chromatography, electrophoretic patterns, and toxic effects among the analyzed samples were identified. Nonetheless, in the preclinical testing of antivenom, two samples from Mera (Pastaza) required a higher dose to achieve total neutralization of lethality and hemorrhage. Taken together, these data highlight the importance of analyzing individual venoms in studies focused on the outcomes of envenoming. © 2021 Elsevier Ltd

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Harlequin frog rediscoveries provide insights into species persistence in the face of drastic amphibian declines

2022 , Jaynes, K.E. , Páez-Vacas, M.I. , Salazar Valenzuela, David , Guayasamin, J.M. , Terán-Valdez, A. , Siavichay, F.R. , Fitzpatrick, S.W.

Amphibians face global declines, and it remains unclear the extent to which species have responded, and through what mechanisms, to persist in the face of emerging diseases and climate change. In recent years, the rediscovery of species considered possibly extinct has sparked public and scientific attention. These are hopeful cases in an otherwise bleak story. Yet, we know little about the population status of these rediscovered species, or the biology underlying their persistence. Here, we highlight the iconic Harlequin frogs (Bufonidae: Atelopus) as a system that was devastated by declines but now encompasses between 18 and 32 rediscoveries (25–37 % of possible extinctions) in the last two decades. Geographic distributions of rediscoveries closely match regional described species abundance, and rediscoveries are documented at elevations from 100 m to >3500 m, with no significant differences between mean historical and contemporary elevations. We also provide genomic data on six decimated species, with historical sample comparisons for two of the species and find a pattern of decreasing genetic variation the longer a species had been missing. Further, we document marked decrease in heterozygosity in one species, but not the other, indicating potential idiosyncratic consequences of declines. Finally, we discuss research priorities to guide the potential transition from amphibian declines to recoveries and to maximize conservation efforts. © 2022 The Authors

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Online toolkits for collaborative and inclusive global research in urban evolutionary ecology

2024 , Amy M. Savage , Meredith J. Willmott , Pablo Moreno‐García , Zuzanna Jagiello , Daijiang Li , Anna Malesis , Lindsay S. Miles , Cristian Román‐Palacios , Salazar Valenzuela, David , Brian C. Verrelli , Kristin M. Winchell , Marina Alberti , Bonilla Bedoya, Santiago , Elizabeth Carlen , Cleo Falvey , Lauren Johnson , Ella Martin , Hanna Kuzyo , John Marzluff , Jason Munshi‐South , Megan Phifer‐Rixey , Ignacy Stadnicki , Marta Szulkin , Yuyu Zhou , Kiyoko M. Gotanda

Urban evolutionary ecology is inherently interdisciplinary. Moreover, it is a field with global significance. However, bringing researchers and resources together across fields and countries is challenging. Therefore, an online collaborative research hub, where common methods and best practices are shared among scientists from diverse geographic, ethnic, and career backgrounds would make research focused on urban evolutionary ecology more inclusive. Here, we describe a freely available online research hub for toolkits that facilitate global research in urban evolutionary ecology. We provide rationales and descriptions of toolkits for: (1) decolonizing urban evolutionary ecology; (2) identifying and fostering international collaborative partnerships; (3) common methods and freely-available datasets for trait mapping across cities; (4) common methods and freely-available datasets for cross-city evolutionary ecology experiments; and (5) best practices and freely available resources for public outreach and communication of research findings in urban evolutionary ecology. We outline how the toolkits can be accessed, archived, and modified over time in order to sustain long-term global research that will advance our understanding of urban evolutionary ecology.