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Alejandra Bonilla-Sánchez, Caroline Charão Sartor, Lester Alexander Fox-Rosales, Anderson Feijó, José D. Ramírez-Fernández, Esteban Brenes-Mora, Michael S. Mooring, Steven R. Blankenship, Catalina Sánchez-Lalinde, Fabio Oliveira do Nascimento, Rebecca Zug, Marcelo Juliano Oliveira, Paulo Henrique Dantas Marinho, Guilherme Braga Ferreira, Sergio Solari, Tadeu Gomes de Oliveira, Eduardo Eizirik
The evolutionary history and taxonomy of the Leopardus tigrinus species complex have been studied based on several approaches, mostly employing genetic and morphological data, leading to distinct classification schemes. We approached this problem from an ecological perspective, with 2 main goals: (i) to evaluate ecological niche differences among regional L. tigrinus populations to determine the extent of ecological divergence among them; and (ii) to identify environmental barriers to historical dispersal that could have driven differentiation among the proposed groups. We modeled the ecological niche of all taxonomic/geographic groups proposed so far to comprise the L. tigrinus complex using the Maximum Entropy algorithm, and evaluated geographic and ecological niche differences among them. Furthermore, we investigated possible environmental barriers to historical dispersal that could have driven differentiation among regional groups. We evaluated 4 hypothetical barriers across 3 time periods to assess their potential historical effect. We found high ecological divergence between northeastern tigrina populations and the northern Andean and Central American tigrinas. Other groups within the L. tigrinus complex are less divergent. In addition, the Guiana Shield tigrina, where the type locality of the species is located, seems to be ecologically similar to populations from northeastern Brazil while also showing some overlap with Andean populations. The Panama center, the Llanos of Colombia and Venezuela, and the Amazon region were identified as historical barriers for tigrina dispersal across all time periods. The inferred historical barriers and ecological divergence observed in this study contribute to the inference of evolutionary differentiation among geographic groups comprising the L. tigrinus complex, revealing areas of consistently low habitat suitability that have likely contributed to divergence among regional populations.
La historia evolutiva y la taxonomía del complejo de especies Leopardus tigrinus se han estudiado en base a varios enfoques, en su mayoría empleando datos genéticos y morfológicos, lo que ha llevado a distintos esquemas de clasificación. Abordamos este problema desde una perspectiva ecológica, con dos objetivos principales: (i) evaluar las diferencias del nicho ecológico entre las poblaciones regionales de L. tigrinus para determinar la existencia de divergencia ecológica entre ellas; e (ii) identificar las barreras ambientales para la dispersión histórica de estos organismos que podrían haber impulsado la diferenciación entre los grupos propuestos. Modelamos el nicho ecológico de todos los grupos taxonómicos/geográficos propuestos hasta ahora para comprender el complejo L. tigrinus utilizando el algoritmo de Máxima Entropía y evaluamos las diferencias geográficas y ecológicas de nicho entre ellos. Además, investigamos posibles barreras ambientales para la dispersión histórica de estos organismos que podrían haber impulsado la diferenciación entre estos grupos regionales. Evaluamos cuatro barreras hipotéticas en tres períodos de tiempo para determinar su posible efecto histórico. Encontramos una alta divergencia ecológica entre las poblaciones de tigrinas del noreste de Brazil y las tigrinas del norte de los andes y centroamericanas. Otros grupos dentro del complejo L. tigrinus son menos divergentes. Además, las tigrinas del Escudo Guayanés, donde se encuentra la localidad tipo de la especie, parece ser ecológicamente similar a las poblaciones del noreste de Brasil, mientras que también muestra cierta superposición con las poblaciones andinas. El centro de Panamá, los Llanos de Colombia y Venezuela y la región amazónica fueron identificados como barreras históricas para la dispersión de tigrinas en todos los períodos de tiempo. Las barreras históricas inferidas y la divergencia ecológica observada en este estudio contribuyen a la inferencia de la diferenciación evolutiva entre los grupos geográficos que comprenden el complejo L. tigrinus, revelando áreas de baja idoneidad para el hábitat que probablemente han contribuido a la divergencia entre estas poblaciones regionales.
Accurate taxonomic species identification is essential to the study of mammals. Despite this necessity, rapid and accurate identification of cryptic, understudied, and elusive mammals remains challenging. Traditional barcoding of mitochondrial genes is standard for molecular identification but requires time-consuming wet-lab methodologies. Recent bioinformatic advancements for nanopore sequencing data offer exciting opportunities for noninvasive and field-based identification of mammals. Nanopore adaptive sampling (NAS), a polymerase chain reaction (PCR)-free method, selectively sequences regions of DNA according to user-specified reference databases. Here, we utilized NAS to enrich mammalian mitochondrial genome sequencing to identify species. Fecal DNA extractions were sequenced from 9 mammals, several collected in collaboration with Minnesota Tribal Nations, to demonstrate utility for NAS barcoding of noninvasive samples. By mapping to the entire National Center for Biotechnology Information mammalian mitochondrial reference genome database and bioinformatically analyzing highly similar matches, we successfully produced species identifications for all fecal samples. Eight of 9 species identifications matched previous PCR or animal/fecal appearance-based identifications. For the ninth species, our genetic data indicate a misidentification stemming from the original study. Our approach has a range of applications—particularly in field-based wildlife research, conservation, disease surveillance, and monitoring of wildlife trade. Of importance to Minnesota tribes is invasive species monitoring, detections, and confirmation as climate impacts cause changes in biodiversity and shifts in species distributions. The rapid assessment techniques described here will be useful as new introductions and range expansions of native and invasive species may first be detected by the presence of signs such as scat rather than direct observations and will be helpful for chronically understaffed tribal natural resources agencies.
The island biogeography theory predicts that species richness in islands and island-like systems is the ultimate result of island isolation and area. Species with high dispersal capabilities are predicted to be less affected by these factors because of their capacity to move more efficiently between islands or habitats, and here we test this idea in bats, the only mammals capable of flight. We conducted mist net and acoustic surveys across 21 islands in the San Juan Archipelago (Washington State, United States) and adjacent northwest mainland to: (i) investigate the effects of island area, distance from mainland, and habitat on bat diversity; and (ii) evaluate whether differences in morphological (body mass, forearm length, wing loading) and ecological (dietary niche breadth, foraging guild) traits among species influence their prevalence across islands. We found that island size strongly influenced patterns of species richness, with larger islands having a greater number of bat species. However, neither island distance from mainland nor any measure of habitat availability was a significant predictor of species richness at the scale of this study. Additionally, we found that dietary niche breadth, as opposed to any morphological trait, best predicted the prevalence of species across the islands. Our results suggest that species with more specialized diets may be more vulnerable to habitat fragmentation, and provide insight into how geographic and ecological factors affect the diversity of insular bat communities, adding to growing knowledge about the role of species traits as mediators of their responses to large-scale landscape structure.
Bats are among the least well-known mammals, particularly in terms of their behavior and activity patterns during the winter. Here, we use passive acoustic monitoring to overcome some of the challenges inherent in surveying cryptic forest bats during the wet season to quantify overwintering behavior for 11 species in California coast redwood forests under varying microclimates. Because different species are active at different forest heights, we also examined the effect of acoustic detector placement (treetop or ground level). Generalized linear mixed models were used to relate acoustic detection probability for 8 species to daytime and nighttime temperature, relative humidity, water vapor pressure, and detector placement. The results indicate that daytime maximum temperature best explained variation in nightly probability of detection, and temperature threshold at which bats were predicted to be detected varied considerably across species. By using more precise species detection methods, we were able to resolve significant differences in activity patterns between Myotis yumanensis and M. californicus, 2 species with similar acoustic signatures that are often lumped together. Myotis californicus was predicted to have a 50% probability of detection at maximum daytime temperature as low as 12.5 °C, whereas M. yumanensis was not predicted to have 50% detection probability until maximum daytime temperature was at least 22 °C, suggesting that M. californicus spends less time in torpor. Also, monitoring at the top of the canopy revealed 4 migratory species to be present in the ecosystem on significantly more monitoring nights than could be observed using conventional ground-based monitoring methods. Improving winter bat survey methods provides evidence that diverse bat species are more active in redwood forests during the winter than previously documented. This finding suggests that coastal forests could provide important winter bat habitat for both resident and migratory species.
The taxonomic status of the Neotropical bat genus Trachops is reevaluated through an integrated study that incorporates morphological, morphometric, and molecular data across its extensive geographic range. Our research, which included previously unexamined geographical regions, revealed substantial insights into the diversity within Trachops. Genetic and morphological results support elevation of T. cirrhosus ehrhardti, distributed within the Atlantic Forest of Brazil, to species status due to differences in southeastern Brazil specimens. Conversely, our analysis found insufficient evidence to maintain the subspecific distinction of T. c. coffini, which lacks diagnosable morphological characters and is not genetically distinct from T. c. cirrhosus across its distribution range. Additionally, our findings challenge a prior notion of latitudinal differentiation in body size in T. cirrhosus, because specimens from western South America and northeastern South America exhibit similar sizes to those from Central America. These results underscore the importance of revising the taxonomic framework for this bat genus—contributing to a more precise understanding of its evolutionary relationships—and further enhancing conservation efforts considering potential threats to the newly recognized species in the imperiled Atlantic Forest of Brazil.
El estatus taxonómico de los murciélagos Neotropicales del género Trachops ha sido reevaluado mediante un estudio integrado que incorpora datos morfológicos, morfométrico y moleculares a través de su extensa distribución geográfica. Nuestra investigación, que incluyó regiones previamente no examinadas, reveló perspectivas sustanciales sobre la diversidad dentro de Trachops. Los resultados respaldan la elevación de T. cirrhosus ehrhardti, distribuido en los Bosques Atlánticos de Brasil, al estatus de especie debido a las diferencias genéticas y morfológicas en especímenes del sudeste de Brasil. Por otro lado, nuestro análisis no encontró suficiente evidencia para mantener la distinción subespecífica de T. c. coffini, que carece de caracteres morfológicos diagnosticables y no difiere genéticamente de T. c. cirrhosus en su rango de distribución. Adicionalmente, nuestros hallazgos confrontan las creencias previas de una diferenciación latitudinal en el tamaño corporal de T. cirrhosus, porque especímenes del oeste y noreste de Sudamérica exhiben tamaños similares a los encontrados en individuos de Centroamérica. Estos resultados subrayan la importancia de examinar el marco taxonómico para este género de murciélagos—contribuyendo a una comprensión más precisa de sus relaciones evolutiva—para aumentar los esfuerzos de conservación a futuro, considerando los riesgos potenciales a la recientemente reconocida especie T. ehrhardti en los Bosques Atlánticos amenazados de Brasil.
North American bat populations have experienced precipitous declines since the introduction of white-nose syndrome (WNS). Evidence that bats have responded to WNS by altering their winter habitat selection has been used to manipulate underground environments and improve winter survival. However, such management practices must be based on local data, which do not exist for all regions. Our goal was to identify determinants of winter habitat use for 3 bat species with varying susceptibility to WNS. To do so, we conducted 188 surveys of 129 potential hibernacula over 3 winters. We found that the range of winter temperatures and presence of water were important for the Little Brown Myotis (Myotis lucifugus) and Tricolored Bat (Perimyotis subflavus), species that are highly susceptible to WNS. Counts of both species were greater in sites with a narrow (<5 °C) temperature range and where streams or water bodies >25 m2 were present. In addition, we found larger groups of Little Brown Myotis in abandoned railroad tunnels than in caves. Winter counts of these species increased over time at 3 railroad tunnels that were surveyed for 3 consecutive winters, whereas populations were extirpated from historically important caves and mines. Counts of Big Brown Bats (Eptesicus fuscus), which are less susceptible to WNS, were also greater in hibernacula with water bodies. However, average winter temperature also helped predict counts of Big Brown Bats. This species had a curvilinear response to temperature, with most bats found at hibernacula with average winter temperatures of 4 to 6 °C, and fewer bats observed at warmer and colder conditions. These data show that focusing solely on historically important hibernacula may fail to achieve conservation goals for the Little Brown Myotis and Tricolored Bat in our region, and suggest that anthropogenic structures can provide habitat for remnant populations of imperiled bat species.
Las poblaciones de murciélagos en Norte América han experimentado un decrecimiento importante desde la introducción del síndrome de la nariz blanca (white-nose syndrome WNS). La evidencia de que los murciélagos han adaptado su comportamiento frente al WNS, cambiando su selección de hábitat durante el invierno, ha sido utilizada para modificar ambientes subterráneos y así mejorar su supervivencia durante el invierno. Sin embargo, estas prácticas de manejo debiesen basarse en datos locales, los cuales son inexistentes para algunas regiones. Nuestro objetivo fue identificar los factores determinantes del uso de hábitat en invierno para tres especies de murciélagos con distinta susceptibilidad al WNS. Para esto, realizamos 188 muestreos en 129 potenciales hibernáculos durante tres inviernos. Observamos que la amplitud de temperaturas y la presencia de agua son factores importantes para Myotis lucifugus y Perimyotis subflavus, especies que son fuertemente impactadas por el WNS. El conteo para ambas especies fue mayor en sitios con una baja amplitud de temperaturas (<5 °C) y con presencia de ríos o cuerpos de agua >25 m2. Adicionalmente, encontramos grupos màs numerosos de Myotis lucifugus en túneles de ferrocarril que en cuevas. Los conteos de invierno para estas especies aumentaron año a año en tres túneles que fueron monitoreados durante tres inviernos consecutivos, mientras que algunas poblaciones fueron erradicadas de cuevas y minas históricamente importantes. El conteo para Eptesicus fuscus, que es menos susceptible al WNS, fue igualmente mayor en hibernáculos con cuerpos de agua, por su parte, la temperatura media en invierno fue un predictor del conteo de individuos para esta especie. Eptesicus fuscus mostró una respuesta curvilínea a la temperatura, con más individuos en hibernáculos con temperaturas medias entre 4 y 6 °C, y menos individuos observados cuando las temperaturas medias eran mayores o menores. Nuestros datos muestran que un enfoque en sitios de hibernación netamente históricos puede no ser el adecuado para lograr objetivos de conservación en nuestra región, y sugieren que estructuras artificiales pueden proveer refugio para poblaciones remanentes de especies de murciélagos en peligro.
Several bat species have experienced rapid population declines in the northern United States and Canada in response to the white-nose syndrome (WNS) epizootic. The pathogen has since spread across the United States, including the Southeast, where relatively warm temperatures may change host–pathogen interactions. In the cave-rich Tennessee–Alabama–Georgia (TAG) region, we examined the impacts of WNS and forest cover on the Tricolored Bat (Perimyotis subflavus) metapopulation using a long-term data set of 832 cave surveys conducted in summer and winter from 2004 to 2022. Most bat colonies were small (<30 individuals), and bats were more likely to be present and abundant in caves surrounded by high percent forest cover, reiterating the importance of forest management for bat conservation. When comparing the years before and after the pathogen arrived in 2010 to 2012, bat presence and abundance during winter hibernation did not change. This stability contrasts with significant declines in other studies, suggesting that Tricolored Bat populations respond differently to WNS in small colonies in the TAG region. Fewer tricolored bats used caves in the summer than during hibernation, but across all years, we observed 1,021 tricolored bats in 121 caves during summer surveys. Unlike stable winter trends, bat presence and abundance declined in the post-WNS period in summer, when cave use is optional. This first broad geographical analysis of summer cave use highlights a potentially important change in bat behavior. Disease surveillance and conservation efforts that target caves with relatively small Tricolored Bat colonies in winter and/or summer may be important for regional population persistence of this threatened species.
Varias especies de murciélagos han experimentado rápidas disminuciones de población en el norte de Estados Unidos y Canadá en respuesta a la epizootia de white-nose syndrome (WNS). Desde entonces, el patógeno se ha extendido por todo Estados Unidos, incluido el sureste, donde las temperaturas relativamente cálidas pueden cambiar las interacciones entre el huésped y el patógeno. En la región de Tennessee–Alabama–Georgia (TAG), rica en cuevas, examinamos los impactos del WNS y la cubierta forestal en la metapoblación del murciélago tricolor (Perimyotis subflavus) utilizando un juego de datos a largo plazo de 832 estudios de cuevas realizados en verano e invierno desde 2004 a 2022. La mayoría de las colonias de murciélagos eran pequeñas (<30 individuos), y era más probable que los murciélagos estuvieran presentes y abundaran en cuevas rodeadas por un alto porcentaje de cubierta forestal, lo que reitera la importancia del manejo forestal para la conservación de los murciélagos. Al comparar los años anteriores y posteriores a la llegada del patógeno en 2010 a 2012, la presencia y abundancia de murciélagos durante la hibernación invernal no cambió. Esta estabilidad contrasta con disminuciones significativas en otros estudios, lo que sugiere que las poblaciones de murciélagos tricolores responden de manera diferente al WNS en pequeñas colonias en la región TAG. Menos murciélagos tricolores usaron cuevas en el verano que durante la hibernación, pero a lo largo de todos los años, observamos 1,021 murciélagos tricolores en 121 cuevas durante los estudios de verano. A diferencia de las tendencias invernales estables, la presencia y abundancia de murciélagos disminuyó en el período posterior al WNS en verano, cuando el uso de cuevas es opcional. Este primer análisis geográfico amplio del uso de las cuevas en verano destaca un cambio potencialmente importante en el comportamiento de los murciélagos. Los esfuerzos de vigilancia y conservación de enfermedades dirigidos a cuevas con colonias de murciélagos tricolores relativamente pequeñas en invierno y/o verano pueden ser importantes para la persistencia de la población regional de esta especie amenazada.
KEYWORDS: Chiroptera, colony size, ecological interactions, functional group, morphology, movement patterns, Chiroptera, grupo funcional, interacciones ecológicas, morfología, patrones de movimiento, tamaño de colonia
Home range is an ecological concept that affects many aspects of the life of vertebrates and hence understanding how it varies between species is crucial. Mammalian home range size has been linked to body size and diet, but these studies were based predominantly on terrestrial species and most specifically excluded bats. As the only group of flying mammals, bats experience distinctly different constraints on movement, and hence home range. However, despite their diversity, relatively little is known about the home ranges of bats, and this is the first global review assessing correlates of their home range size. Our hypothesis is that home range will be impacted by different ecological conditions experienced by the bats and by the biological traits of the bats themselves. We performed a meta-analysis based on published data for 81 bat species to identify variables that contribute most to home range size. Sex, wing loading, functional group, colony size, dietary class, distance from the equator (latitudinal region), habitat type, and the interaction between habitat type and latitudinal region were all important explanatory variables. Wing loading was positively correlated with home range size—while females, open-air foragers, large colony sizes, and bats in temperate regions consistently had large home ranges. Understanding the correlates of home range has important implications, for example, for bat conservation and for assessing the risk of spillover of zoonotic pathogens from bats to humans and livestock.
El ámbito de hogar es un concepto ecológico que influye en muchos aspectos de la vida de los vertebrados, por lo que es fundamental comprender el modo en que varía entre especies. El ámbito de hogar de los mamíferos ha sido relacionado con el tamaño corporal y la alimentación, pero esos estudios se basaban principalmente en especies terrestres y, concretamente, excluían a los murciélagos. Al ser el único grupo de mamíferos voladores, los murciélagos experimentan restricciones de movimiento diferenciales y en consecuencia sus ámbitos de hogar también varían. Sin embargo, a pesar de su diversidad, el conocimiento de los ámbitos de hogar de los murciélagos es escaso, y esta es la primera revisión global que evalúa la variables que se correlación con el tamaño de sus ámbitos hogareños. Nuestra hipótesis establece el ámbito de hogar de los murciélagos está influenciado por sus características biológicas y por las diferentes condiciones ecológicas que experimentan. Desarrollamos un metanálisis en función de la información publicada sobre 81 especies de murciélagos para identificar las variables que más influyen en el tamaño del ámbito de hogar. El sexo, la carga alar, el grupo funcional, el tamaño de la colonia, la clase de alimentación, la distancia hasta el ecuador (zona latitudinal), el tipo de hábitat y la interacción entre este y la zona latitudinal fueron consideradas como variables explicativas importantes. La carga alar mostró una correlación positiva con el tamaño del ámbito de hogar, mientras que las hembras, los murciélagos forrajeadores de espacios abiertos, las colonias de gran tamaño y los murciélagos de zonas templadas tuvieron ámbitos de hogar consistentemente grandes. La comprensión de las variables que se correlacionan con el ámbito de hogar tiene repercusiones importantes, por ejemplo, para la conservación de los murciélagos y el estudio del riesgo de propagación de patógenos zoonóticos de los murciélagos hacia los humanos y el ganado.
KEYWORDS: habitat use, niche breadth, range extension, secondary succession, tri-colored bat, Amplitud de nicho, extensión del rango, murciélago tricolor, sucesión secundaria, uso de hábitat
Several studies have indicated that tri-colored bats (Perimyotis subflavus) are extending their distributional range westward in the United States. Montane and subalpine habitats consist of a mosaic of forest types including Lodgepole Pine woodlands and meadows, which provide an opportunity to study how a newly arriving species—typically associated with lowland riparian systems—is adapting to novel environmental conditions. The objectives of this study are to document Tri-colored Bat activity in these novel habitats and to quantify which factors are influencing activity patterns in habitats and at elevations not previously documented. We surveyed sites in various stages of secondary succession following beetle kill outbreaks using acoustic monitoring and nonparametric multiplicative regression to model habitat activity patterns. Results showed that activity was highest in meadows and early time-since-kill (TSK) forests in the beginning of the survey period and activity increased in late TSK forest habitats at the end of the survey in early August. Tri-colored bats are not restricting their activity to lower-elevational riparian areas in the Colorado foothills but appear to also be using these high-elevation habitats. Careful consideration of misidentification confirms the high likelihood of tri-colored bats at our sites. We hope that this study will support conservation efforts considering the expected US Fish and Wildlife Service Endangered listing for this species.
Varios estudios han indicado que los murciélagos tricolor (Perimyotis subflavus) están ampliando hacia el occidente su rango distribucional en los Estados Unidos. Los hábitats de montaña y subalpinos consisten de un mosaico de bosques que incluyen bosques de pino contorto y prados, que ofrecen la oportunidad de estudiar la forma en que una especie recién llegada, típicamente asociada con sistemas ribereños de tierras bajas, se está adaptando a condiciones ambientales novedosas. Los objetivos de este estudio son documentar la actividad del murciélago tricolor en estos nuevos hábitats y cuantificar cuales factores influyen los patrones de actividad a elevaciones y en hábitats donde no se han documentado anteriormente. Seleccionamos sitios que se hallaban en diversas etapas de sucesión secundaria tras brotes mortíferos de escarabajos. Utilizamos monitoreo acústico para modelar los patrones de actividad en el hábitat utilizando regresiones multiplicativas no paramétricas. Los resultados mostraron que la actividad del murciélago tricolor al principio de la encuesta estaba en su máximo en los prados y en los bosques con poco-tiempo-post-muerte, TSK por su sigla en inglés y que la actividad aumentó en los hábitats boscosos con TSK tardía hacia la conclusión del período de la encuesta, a principios de agosto. Los murciélagos tricolor no restringen su actividad a las zonas ribereñas de baja altitud en el piedemonte de Colorado sino parece ser que también utilizan estos hábitats de mayor altitud. Una cuidadosa consideración de identificaciones erróneas confirma la alta probabilidad de la presencia de murciélagos tricolor en nuestros sitios. Esperamos que este estudio apoye los esfuerzos de conservación para esta especie, tomando en cuenta la expectativa de que El Departamento de Pesca y Vida Silvestre de los Estados Unidos la incluirá en la lista de especies en Peligro de Extinción.
The genus Notiosorex is the only group of shrews in North America with adaptations to arid or semiarid zones. The genus was described with a single variable species, Notiosorex crawfordi, from which 5 new species have since been distinguished. To date, the phylogenetic relationships of Notiosorex species have only been partially analyzed and it is possible that there are still distinct species included within the catch-all of N. crawfordi. Here, we use geometric morphometrics on cranial and mandibular characters of the described extant species, 3 fossil species, and a distinctive population of N. crawfordi as a proxy for an integrated assessment of phylogenetic relationships of all Notiosorex species. Our results indicate that the population from the Altiplano Mexicano is more similar to, yet distinct from, N. villai than it is to N. crawfordi—we describe it as a new species. We also used the resulting tree to reconstruct phylogeographic history within the genus, which suggests that Notiosorex sp. nov., N. villai, N. evotis, and N. tataticuli all diverged allopatrically as populations from the ancestral area that is currently occupied by N. crawfordi (and in the deeper past by the fossil species N. harrisi), and pushed south into the Gulf Coast, the Altiplano, and Baja California within the last 5 million years following the end of the Miocene.
El género Notiosorex es el único grupo de musarañas con adaptaciones a zonas áridas y semiáridas en Norteamérica. El género fue descrito con base en una sola especie muy variable, Notiosorex crawfordi; desde ese entonces, se han descrito cinco nuevas especies. Hasta la fecha, las relaciones filogenéticas de las especies dentro del género Notiosorex solo han sido analizadas parcialmente, y es posible que haya aún mayor número de especies nuevas incluidas dentro del grupo general de N. crawfordi. En este estudio, utilizamos morfometría geométrica del cráneo y mandíbula de las especies vivas ya descritas, además de tres especies fósiles, y una población distintiva de N. crawfordi del Altiplano Mexicano como un indicador para una evaluación integrada de las relaciones filogenéticas de todas las especies de Notiosorex. Nuestros resultados indican que la población del Altiplano Mexicano es más similar y claramente diferenciable de N. villai que de N. crawfordi, y la describimos como una nueva especie. Utilizamos el árbol filogenético para reconstruir la historia filogeográfica del género, lo que sugiere que esta nueva especie del Altiplano, junto con N. villai, N. evotis y N. tataticuli, todas divergieron de forma alopátrica como poblaciones separadas a partir de la zona ancestral que actualmente ocupa N. crawfordi (y en el pasado más antiguo, por la especie fósil N. harrisi) y se desplazaron hacia el sur, hacia la costa del Golfo, el Altiplano y Baja California en los últimos 5 millones de años, desde finales del Mioceno.
Interspecific competition, environmental filtering, or spatial variation in productivity can contribute to positive or negative spatial covariance in the abundances of species across ensembles (i.e., groups of interacting species defined by geography, resource use, and taxonomy). In contrast, density compensation should give rise to a negative relationship between ecomorphological similarity and abundance of species within ensembles. We evaluated (1) whether positive or negative covariances characterized the pairwise relationships of 21 species of Congolese shrew, and (2) whether density compensation characterized the structure of each of 36 Congolese shrew ensembles, and did so based on the abundances or biomasses of species. In general, positive covariance is more common than negative covariance based on considerations of abundance or biomass, suggesting dominant roles for environmental filtering and productivity. Nonetheless, negative covariance is more common for ecomorphologically similar species, suggesting a dominant role for competition within functional groups. Effects of abundance or biomass compensation, via pairwise or diffuse competitive interactions, were detected less often than expected by chance, suggesting that interspecific competition is not the dominant mechanism structuring these ensembles. Effects of competition may be balanced by responses to variation in resource abundance among sites in a landscape or among niche spaces within sites. Future studies of compensatory effects should incorporate considerations of heterogeneity in the abundance and distribution of resources in ecological space to better isolate the effects of competition and resource abundance, which can have opposing effects on community structure.
Both natural and anthropogenic forces can play a substantial role in the demographic history and current structure of a wildlife population. Species with strict habitat requirements are especially susceptible to these impacts. Mountain goats (Oreamnos americanus) in Alaska are of particular interest in this regard due to their influence on alpine ecosystems, importance to human cultures, and enigmatic history in some areas. Here, we used genetic tools to examine the population structure and demographic history of mountain goats in Alaska. We genotyped 816 mountain goats at 18 microsatellites, identified the number of genetically distinct subpopulations, and assessed their genetic diversity. We used Bayesian methods to investigate demographic history relative to the known geologic and human history of Alaska, and we simulated human-mediated translocation events onto islands to address the hypothesis that Baranof Island harbored an extant population prior to an early 20th-century introduction. We showed that Alaska has 4 genetically distinct subpopulations of mountain goats. The main demographic split between Southcentral and Southeast Alaska occurred following the retreat of ice after the Last Glacial Maximum. Simulations of translocation events largely aligned with expected genetic diversity patterns of current subpopulations except for Baranof Island which showed greater diversity than the simulation, consistent with the hypothesis of an endemic population prior to the translocation. This study highlights the value of considering both natural and anthropogenic forces when assessing the biogeographic history of a species and provides new insights about the complex demographic history and biogeography of mountain goats in Alaska.
Seasonal reproduction is an adaptive strategy that benefits the survival and growth of offspring. However, the regulatory mechanisms affecting spermatogenesis in male seasonal breeders are not well understood. We examined the actions of testosterone on seasonal spermatogenesis of Plateau Pika (Ochotona curzoniae), a typical long-day breeder living on the Qinghai–Tibetan Plateau. The annual dynamics of germ cell development and steroid hormone synthesis were confirmed and were consistent with testicular morphology. Furthermore, a testosterone regulation experiment showed that elevated testosterone stimulated proliferation of spermatogonia and regeneration of advanced spermatogenic cells in reproductively dormant pika, while testosterone suppression induced cell apoptosis both in reproductively active and dormant pikas. Transcriptomic analyses indicated that testosterone-regulated genes related to spermatogonial fate determination by binding to androgen receptors and inducing the production of retinoic acid, which was responsible for the initiation of spermatogonial differentiation. We show that testosterone orchestrates downstream signaling pathways to balance spermatogonial self-renewal and development. These findings provide a new perspective on seasonal regulation of mammalian spermatogenesis.
Population density is a potentially significant determinant of social organization, with high densities often expected to result in greater spatial and social contact among conspecifics. As part of ongoing efforts to document behavioral diversity among tuco-tucos (Rodentia: Ctenomyidae: Ctenomys), we characterized the social organization of a population in Valle Encantado, Parque Nacional Los Cardones, Salta Province, Argentina. Live-trapping and radiotelemety data revealed that despite one of the highest densities recorded for the genus Ctenomys (∼75 adults per ha), members of the study population were solitary, with each adult occupying a distinct burrow system and nest site. Co-occurrence of adults at the same point in space and time was detected only twice (<0.5% of data points, n = 997 telemetry fixes). Spatial overlap between neighboring animals was limited and resulted from occasional incursions by 1 individual into the area occupied by a conspecific, with most (87.5%, n = 8) such events occurring when an adult male entered the area occupied by an adult female. Comparisons with other species of Ctenomys for which telemetry data are available did not suggest a relationship between population density and social organization within this genus. Although a formal taxonomic assessment of the tuco-tucos from Valle Encantado is needed, our findings add to a growing comparative understanding of variation in social organization within Ctenomys.
La densidad poblacional es un factor potencialmente significativo que determinar la organización social, ya que se espera que densidades elevadas resulten en una mayor interacción espacial y social entre conspecíficos. Como parte de esfuerzos continuos para documentar la diversidad de comportamiento entre los tuco-tucos (Rodentia: Ctenomyidae: Ctenomys), caracterizamos la organización social de una población de estos animales en el Valle Encantado, Parque Nacional Los Cardones, Salta, Argentina. Las capturas vivas y los datos de telemetría revelaron que, a pesar de tener una de las densidades más altas registradas entre los Ctenomys (∼75 adultos por hectárea), los miembros de la población estudiada eran solitarios, ocupando cada adulto su propio sistema de túneles y nidos. La co-ocurrencia espacial y temporal de adultos en el mismo sitio solo se detectó en dos ocasiones (<0.5% de las posiciones, N = 997 localizaciones telemétricas). El solapamiento espacial entre animales vecinos fue limitado y resultó de incursiones ocasionales de un individuo en el área ocupada por un conspecífico, con la mayoría (87.5%, N = 8) de estos eventos ocurriendo cuando un macho adulto ingresaba en el área ocupada por una hembra adulta. Las comparaciones con otras especies de Ctenomys para las cuales hay disponibilidad de datos telemétricos no sugieren una relación entre la densidad poblacional y la organización social dentro del género. Los análisis de una porción de 801 pares de bases del locus mitocondrial citocromo-b indican que los tuco-tucos del Valle Encantado forman una unidad monofilética que no es parte de ninguno de los subclados reconocidos actualmente dentro del género Ctenomys, lo que sugiere la necesidad de una evaluación taxonómica formal de estos animales.
Artificial light at night is increasingly recognized as a cause of habitat degradation, and as a conservation threat to wildlife species. We studied the behavioral response of Pacific kangaroo rats (Dipodomys agilis) to natural and artificial light in coastal sage scrub in southern California, United States. We used digital trail cameras to monitor visits to seed trays in shrub and open, intershrub microhabitats. Under natural-light conditions, kangaroo rats were more active on full- than new-moon nights, and concentrated foraging beneath shrubs. Surprisingly, kangaroo rats frequently interacted with other rodents in seed trays. Near to an artificial light source, kangaroo rats removed fewer seeds, had fewer foraging bouts, and spent less time in trays—especially in brightly lit open microhabitats—compared to distances farther from the light. Differences between the first and second nights of trials during both experiments suggested that kangaroo rats learned locations of resource-rich seed trays and modified their behavior accordingly. Our results are similar to recent studies showing that artificial light depresses foraging activity of rodents in the areas of highest illumination, and adds to evidence of the need to mitigate impacts of urban lighting in fragments of coastal sage scrub, especially along the urban–wildland interface.
Space use by small mammals should mirror their immediate needs for food and predator shelters but can also be influenced by seasonal changes in biotic and abiotic factors. Lemmings are keystone species of the tundra food web, but information on their spatial distribution in relation to habitat heterogeneity is still scant, especially at a fine scale. In this study, we used spatially explicit capture–recapture methods to determine how topography, hydrology, vegetation, and soil characteristics influence the fine-scale spatial variations in summer density of brown lemmings (Lemmus trimucronatus). Lemmings were monitored throughout the summer in wet and mesic tundra habitats and in a predator exclusion grid, which was also located in mesic tundra. We found that in wet tundra, lemming densities were higher at sites with a rugged topography dominated by hummocks, but only during snow melt. In both mesic tundra sites, lemming densities were higher in sites with poor drainage and low aspect throughout the summer. We found no clear association between lemming densities and any tested vegetation or soil variables. Overall, hydrology and topography appear to play a dominant role in small-scale space use of brown lemmings with a secondary role for predator avoidance and food plant abundance.
L'utilisation de l'espace par les petits mammifères devrait refléter leurs besoins immédiats de nourriture et de protection des prédateurs, mais elle peut aussi être influencée par des changements saisonniers dans les facteurs biotiques et abiotiques. Les lemmings sont des espèces clés dans le réseau alimentaire de la toundra, pourtant les connaissances sur leur répartition spatiale en relation avec l'hétérogénéité des habitats sont limitées, surtout à fine échelle spatiale. Dans cette étude, nous avons utilisé des méthodes de captures-recaptures spatialement explicites pour déterminer comment la topographie, l'hydrologie, la végétation et les caractéristiques des sols influencent les variations à fine échelle spatiale des densités estivales de lemmings bruns (Lemmus trimucronatus). Les lemmings ont été suivis tout au long de l'été dans des habitats de toundra humide et mésique et dans une grille d'exclusion des prédateurs qui se situait aussi en toundra mésique. Nous avons constaté que dans la toundra humide, les densités de lemmings étaient plus élevées dans les sites avec une topographie accidentée dominée par des hummocks, mais seulement pendant la fonte de la neige en juin. Dans les deux sites en toundra mésique, les densités de lemmings étaient plus élevées là où la pente était faible et le drainage mauvais pendant tout l'été. Nous n'avons trouvé aucun effet des variables végétales ou des sols que nous avons testées. Dans l'ensemble, l'hydrologie et la topographie semblent jouer un rôle prépondérant dans l'utilisation de l'espace par le lemming brun à fine échelle, alors que l'évitement des prédateurs et l'abondance des plantes fourragères auraient un rôle secondaire.
Jonathan R. Argov, Nesha B. Michaels, Rachel A. Smiley, Brittany L. Wagler, Jack N. Gavin, Alyson B. Courtemanch, Dean Clause, Rusty C. Kaiser, Daryl Lutz, Brandon Scurlock, Kevin L. Monteith
Reproductive phenology is a critical element of how animals persist in their environment and affects survival of young, especially in seasonal environments. We investigated the correlation between fetal eye diameter and birth timing to determine if birthdates could be predicted by a prenatal metric. We used ultrasonography to measure eye diameters of fetuses and vaginal implant transmitters to determine birthdates of Rocky Mountain Bighorn Sheep (Ovis canadensis canadensis) in Wyoming, United States, from 2019 to 2023. Fetal eye diameter strongly predicted days until birth (β = –2.8; pseudo-R2 = 0.88). Effective prediction of birthdates via ultrasonography can yield opportunities for logistical planning in neonatal studies, monitoring changes in reproductive phenology, and evaluating questions of resource allocation relative to reproductive processes.
La fenología reproductiva es un elemento crítico de cómo los animales persisten en su entorno y afecta a la supervivencia de las crías, especialmente en ambientes estacionales. Investigamos la correlación entre el diámetro ocular del feto y el momento del nacimiento para determinar si las fechas de nacimiento podrían predecirse mediante una métrica prenatal. Utilizamos la ecografía para medir los diámetros oculares de los fetos y los transmisores de implantes vaginales para determinar las fechas de nacimiento del borrego cimarrón de las Montañas Rocosas (Ovis canadensis canadensis) en Wyoming, EE. UU., de 2019 a 2023. El diámetro ocular fetal predijo firmemente los días hasta el nacimiento (β = –2,8; pseudo-R2 = 0,88). La predicción eficaz de las fechas de nacimiento mediante ecografía puede generar oportunidades para la planificación logística en estudios neonatales, el seguimiento de los cambios en la fenología reproductiva y la evaluación de preguntas de asignación de recursos en relación con los procesos reproductivos.
It is commonly recognized that predation and the risk of predation can have profound effects on behaviors and population ecology of prey. Comparatively, little attention has been paid to the trade-offs hosts make to manage the risk of parasitism, but there is evidence that hosts make behavioral trade-offs to avoid parasitism in ways that resemble those made by prey animals under the risk of predation. Mosquitoes are common hematophagous ectoparasites which parasitize a wide range of vertebrates, resulting in blood loss, distraction, and disease transmission. Many hosts engage in defensive behaviors to repel or kill mosquitoes and these behaviors likely come at the expense of activities such as foraging and vigilance for predators. We placed a mosquito attractant (BG-Sweetscent) and repellant (allethrin) near artificial foraging patches in areas where mosquitoes were common and measured the amount of grain left after a night of foraging (giving-up density) to investigate whether mosquitoes influenced Cotton Mouse (Peromyscus gossypinus) foraging. We predicted that in patches with mosquito attractants, mosquito harassment would cause mice to engage in defensive behaviors which would distract or deter them from foraging, resulting in less grain consumption relative to control patches. Conversely, we predicted that in mosquito-repellent patches, mice would experience less harassment, resulting in more grain consumption. Indoor arena trials found no evidence that the mosquito treatments influenced cotton mouse behavior in the absence of mosquitoes. However, we found no evidence that mosquito treatments affected giving-up densities.
Moose (Alces alces) in boreal habitats feed and rest where they are exposed to Dipteran flies and the parasites they carry. We collected 31,905 flies during the summer from 12 habituated moose on the Kenai Peninsula, Alaska. Moose flies, Haematobosca alcis (Snow), Diptera: Muscidae—a species that completes its entire life cycle on or around moose—accounted for 91% of flies collected; the reminder of the flies collected included mosquitoes (Culicidae), black flies (Simuliidae), and deer flies (Tabanidae). Flies impose physiological costs for moose, e.g., vectors for parasites such as Legworm (Onchocerca spp.) which causes sores on the hind legs of moose. We found that the number of sores present on the hind legs of moose is positively correlated with body fat, which suggests a correlation between gains of energy and damage from flies. We also found that the number of sores is negatively correlated with serum albumin, which is indicative of an inflammatory response and body protein being used to repair injuries from flies and parasites. The number or type of flies present on a Moose were not correlated with the concentration of corticosteroids in saliva or feces. Flies do not elicit a stress response in moose even though the costs of repairing wounds and resisting infections of those wounds likely reduce gains of protein from summer foraging. Moose can tolerate the injuries from biting flies with regular gains from summer foraging but exposure to insect-borne parasites poses a risk to reproduction and survival.
Wildlife disease outbreaks can lead to population declines, which are usually attributed to increased direct or indirect mortality. Alternatively, behavior associated with sickness can lead to social isolation, potentially decreasing fitness of affected individuals. A useful case study to examine this dynamic is chronic wasting disease (CWD), a neurological disease of cervids, known to affect behavior and movement. In this study, we monitored scraping, a White-tailed Deer (Odocoileus virginianus; WTD) breeding season behavior, in an area of high CWD prevalence to determine if this reproductive behavior is affected by CWD. At 107 scrape sites, we detected 3,063 scrape interactions and 218 unique bucks. Bucks engaged with scrapes most often, performing 73% of interactions—compared to 23% by does, and 4% by fawns. Twenty-one bucks captured on camera traps at scrape sites were harvested through recreational hunting, 13 testing CWD-positive and 8 CWD not-detected. We found no significant effect of CWD status on specific scraping behaviors. There may, however, have been population-level effects, with shifts toward greater proportions of scraping by yearling bucks and during daylight hours compared to findings from past studies.
Mother–offspring communication is especially crucial for social species in order to synchronize activities essential for early survival including nursing, resting, maintaining proximity during group movements between food or water sources, and locating one another if separated in a large social group. One of the most social ungulate species in North America is the American Bison (Bison bison), formerly known as buffalo. Adult female bison associate with their young for over a year and communication between mother and offspring is likely essential for establishing and maintaining a bond upon which the life of a calf depends. One goal of this study was to quantify and compare the acoustic form of vocalizations of adult female, subadult, and calf bison and to determine how age classes differed in call structure. The other goal was to identify the contexts in which bison vocalized. Vocalizations of 101 bison (53 adult females, 15 subadults, 33 calves) in a semi-free-ranging herd in Montana were analyzed and found to be pulsatile sounds, unlike vocalizations of bison bulls or domestic cows and calves. Vocalizations of bison cows, subadults, and calves differed significantly in total duration, numbers of pulses, pulse duration, and pulse rate. Seven distinct call contexts were identified. The majority of calls were “moving-on calls” (39%), when a cow called and her calf ran to her side and the 2 moved on together, and “contact calls” (21%) when a cow called and her calf called back but neither changed their location. “Imprinting calls” and “nursing calls” were also identified. Mother–offspring acoustic communication in bison appears especially critical for coordinating movements. Understanding the role of acoustic communication in maintaining the bond between bison mothers and their offspring can contribute to the humane management and welfare of this iconic species.
La comunicación madre-cría es especialmente crucial para especies sociales, debido a que permite sincronizar actividades esenciales para la supervivencia temprana, como la lactancia, el descanso, el mantenimiento de proximidad durante los movimientos de los grupo entre las fuentes de alimento o agua y la localización mutua en caso de separación dentro de un grupo social grande. Una de las especies de ungulados más sociales de América del Norte es el bisonte (Bison bison). Las hembras adultas de bisonte se asocian con sus crías durante más de un año y la comunicación entre madre el becerro es probablemente esencial para establecer y mantener un vínculo en el que depende la vida de la cría. Uno de los objetivos de este estudio fue cuantificar y comparar la forma acústica de las vocalizaciones de hembras adultas, subadultas y crías de bisonte, y determinar cómo diferían las clases por edad en la estructura de las llamadas. Otro objetivo fue identificar los contextos en los que se emitían las vocalizaciones. Se analizaron las vocalizaciones de 101 bisontes (53 hembras adultas, 15 hembras subadultas, 33 crías) en un rebaño semi-libre en Montana. Se encontró que estas vocalizaciones eran sonidos pulsátiles, completamente diferentes a los emitidos por los bisontes machos adultos o las vacas y becerros domésticos. Las vocalizaciones diferían significativamente entre las tres clases de edad en su duración total, número de pulsos, duración de los pulsos y ritmo de los pulsos. La mayoría de las llamadas se dieron en dos contextos: “llamadas de avance” (39%), cuando una hembra adulta llamaba y su cría corría a su lado y ambas avanzaban juntas, y “llamadas de contacto” (21%), cuando una hembra adulta llamaba y su cría respondía, pero ninguna cambiaba su ubicación. También se identificaron “llamadas de impronta” y “llamadas de amamantamiento,” así como otros tres contextos de llamada. La comunicación acústica madre-cría en bisontes parece especialmente crítica para coordinar los movimientos. Entender el papel de la comunicación acústica en el mantenimiento del vínculo entre las madres y sus crías puede contribuir al manejo humanitario y al bienestar de esta especie icónica. Este trabajo representa el primer estudio que investiga cuantitativamente las señales acústicas de hembras adultas, subadultas y crías de bisontes Norte Americanos mientras se desplazan en condiciones de semi-libertad.
During a limited period in the summer of 2021, 17-year cicada species (Magicicada cassini, M. septendecula, M. septendecim) represented a large pulse of easily accessible food unique to forest ecosystems in the eastern United States. Using trail cameras and acoustic recorders, we tested whether the activity levels of 8 mammal species in northwestern Indiana shifted in response to spatial and temporal variation in cicada densities from 18 May to 20 June 2021. Cicada densities varied temporally and spatially across all study sites. Most mammal species with sufficient data showed no response to cicada emergence, including 2 tree squirrel species, Peromyscus mice, Eastern Chipmunks (Tamias striatus), and 2 species of bats. Raccoons (Procyon lotor), likely cicada predators, showed a quadratic or more complex activity response to cicada abundance, indicating a potential saturation point at densities near 1 cicada per m2. Surprisingly, White-tailed Deer (Odocoileus virginianus) activity decreased to almost 0 at the same cicada densities when we expected no change in activity. While size or accessibility may exclude cicadas as prey for small and volant mammals, our results suggest predation and satiation by Raccoons. In contrast, deer may be avoiding areas of cicada abundance due to other stimuli, such as high noise output, which may decrease their ability to detect predators.
Molting is an evolutionarily ancient trait in which the outermost layer of an organism is replenished, usually according to a regular circannual rhythm. It is a metabolically costly process and, in vertebrates, is generally timed around other energetically demanding events such as reproduction and migration. In mammals, molting involves replacement of the fur coat—one of the most distinct innovations of the mammalian lineage. Despite the obvious importance of hair to mammalian fitness, our knowledge of hair growth cycles, circannual molting patterns, and hair structure remains largely restricted to marine and domesticated mammals, and our ability to identify explicit adaptive advantages of molting strategies in any mammal is therefore limited. In this review, we summarize what is known of these topics in wild, terrestrial mammals with a particular emphasis on marmots (Marmota spp.). Marmots are the largest extant ground squirrels and are well adapted to seasonally cold environments. Molting may be particularly relevant to fitness in marmots given the presumed importance of a healthy, insulative coat for metabolic efficiency in cold environments. Moreover, marmots hibernate for 7 to 8 months each year, meaning the annual molt and all other energetically demanding life-history events (such as parturition, lactation, fat accumulation, and dispersal) are constrained to an active period of only 4 to 5 months. Because the energetics of hibernation, fat accumulation, reproduction, and social behavior are already well studied, examining how molt is timed with respect to other important events and how it is influenced by local conditions may inform how molting is prioritized and how molting strategies evolve under specific selective pressures.
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