Salazar Valenzuela, David
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Preferred name
Salazar Valenzuela, David
Main Affiliation
Quito
Email
davidsalazar@uti.edu.ec
ORCID
Scopus Author ID
26644312900

Research Output
Now showing 1 - 10 of 27
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Resistance Is Not Futile: Widespread Convergent Evolution of Resistance to Alpha-Neurotoxic Snake Venoms in Caecilians (Amphibia: Gymnophiona)

2023 , Mancuso M. , Zaman S. , Maddock S.T. , Kamei R.G. , Salazar Valenzuela, David , Wilkinson M. , Roelants K. , Fry B.G.

Predatory innovations impose reciprocal selection pressures upon prey. The evolution of snake venom alpha-neurotoxins has triggered the corresponding evolution of resistance in the post-synaptic nicotinic acetylcholine receptors of prey in a complex chemical arms race. All other things being equal, animals like caecilians (an Order of legless amphibians) are quite vulnerable to predation by fossorial elapid snakes and their powerful alpha-neurotoxic venoms; thus, they are under strong selective pressure. Here, we sequenced the nicotinic acetylcholine receptor alpha-1 subunit of 37 caecilian species, representing all currently known families of caecilians from across the Americas, Africa, and Asia, including species endemic to the Seychelles. Three types of resistance were identified: (1) steric hindrance from N-glycosylated asparagines; (2) secondary structural changes due to the replacement of proline by another amino acid; and (3) electrostatic charge repulsion of the positively charged neurotoxins, through the introduction of a positively charged amino acid into the toxin-binding site. We demonstrated that resistance to alpha-neurotoxins convergently evolved at least fifteen times across the caecilian tree (three times in Africa, seven times in the Americas, and five times in Asia). Additionally, as several species were shown to possess multiple resistance modifications acting synergistically, caecilians must have undergone at least 20 separate events involving the origin of toxin resistance. On the other hand, resistance in non-caecilian amphibians was found to be limited to five origins. Together, the mutations underlying resistance in caecilians constitute a robust signature of positive selection which strongly correlates with elapid presence through both space (sympatry with caecilian-eating elapids) and time (Cenozoic radiation of elapids). Our study demonstrates the extent of convergent evolution that can be expected when a single widespread predatory adaptation triggers parallel evolutionary arms races at a global scale. © 2023 by the authors.

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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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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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A new species of harlequin toad (Bufonidae: Atelopus) from Amazonian Ecuador

2024 , Plewnia, Amadeus , Terán-Valdez, Andrea , Culebras, Jaime , Boistel, Renaud , Paluh, Daniel J. , Quezada Riera, Amanda B. , Salazar Valenzuela, David , Guayasamin, Juan Manuel

For nearly four decades, harlequin toads, genus Atelopus, have suffered unparalleled population declines. While this also results in limited understanding of alphataxonomic relationships, these toads face an urgent need for advances in systematics to inform conservation efforts. However, high intraspecific variation and cryptic diversity have hindered a comprehensive understanding of Atelopus diversity. This is particularly exemplified among Amazonian populations related to A. spumarius, where decades of taxonomic work have not been able yet to unravel relationships between the many forms, while the names coined so far have led to taxonomic confusion leaving numer-ous lineages unnamed. A recent comprehensive phylogenetic study has revealed new insights into the systematics of harlequin toads with an emphasis on Amazonian forms, identifying several unnamed lineages. We here describe one of these evolutionary lineages as a new species, restricted to the Ecuadorian Amazon basin, in an integrative taxonomic approach using molecular, morphological, bioacoustic and larval information. With this, we contribute to a better understanding of Atelopus diversity as the baseline of conservation action.

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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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A new species of harlequin toad (Bufonidae: Atelopus) from Amazonian Ecuador

2024 , Plewnia, Amadeus , Terán-Valdez, Andrea , Culebras, Jaime , Boistel, Renaud , Paluh, Daniel , Quezada Riera, Amanda B. , Heine, Christopher H , Reyes-Puig, Juan , Salazar Valenzuela, David , Guayasamin, Juan Manuel

For nearly four decades, harlequin toads, genus Atelopus, have suffered unparalleled population declines. While this also results in limited understanding of alphataxonomic relationships, these toads face an urgent need for advances in systematics to inform conservation efforts. However, high intraspecific variation and cryptic diversity have hindered a comprehensive understanding of Atelopus diversity. This is particularly exemplified among Amazonian populations related to A. spumarius, where decades of taxonomic work have not been able yet to unravel relationships between the many forms, while the names coined so far have led to taxonomic confusion leaving numer-ous lineages unnamed. A recent comprehensive phylogenetic study has revealed new insights into the systematics of harlequin toads with an emphasis on Amazonian forms, identifying several unnamed lineages. We here describe one of these evolutionary lineages as a new species, restricted to the Ecuadorian Amazon basin, in an integrative taxonomic approach using molecular, morphological, bioacoustic and larval information. With this, we contribute to a better understanding of Atelopus diversity as the baseline of conservation action.

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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.

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First Insights into the Venom Composition of Two Ecuadorian Coral Snakes

2022 , Hernández-Altamirano, J.A. , Salazar Valenzuela, David , Medina-Villamizar, E.J. , Quirola, D.R. , Patel, K. , Vaiyapuri, S. , Lomonte, B. , Almeida, J.R.

Micrurus is a medically relevant genus of venomous snakes composed of 85 species. Bites caused by coral snakes are rare, but they are usually associated with very severe and life-threatening clinical manifestations. Ecuador is a highly biodiverse country with a complex natural environment, which is home to approximately 20% of identified Micrurus species. Additionally, it is on the list of Latin American countries with the highest number of snakebites. However, there is no local antivenom available against the Ecuadorian snake venoms, and the biochemistry of these venoms has been poorly explored. Only a limited number of samples collected in the country from the Viperidae family were recently characterised. Therefore, this study addressed the compositional patterns of two coral snake venoms from Ecuador, M. helleri and M. mipartitus, using venomics strategies, integrating sample fractionation, gel electrophoresis, and mass spectrometry. Chromatographic and electrophoretic profiles of these snake venoms revealed interspecific variability, which was ascertained by mass spectrometry. The two venoms followed the recently recognised dichotomic toxin expression trends displayed by Micrurus species: M. helleri venom contains a high proportion (72%) of phospholipase A2, whereas M. mipartitus venom is dominated by three-finger toxins (63%). A few additional protein families were also detected in these venoms. Overall, these results provide the first comprehensive views on the composition of two Ecuadorian coral snake venoms and expand the knowledge of Micrurus venom phenotypes. These findings open novel perspectives to further research the functional aspects of these biological cocktails of PLA2s and 3FTxs and stress the need for the preclinical evaluation of the currently used antivenoms for therapeutic purposes in Ecuador. © 2022 by the authors.

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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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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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