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Additional file 1: Figure S1. Flea cumulative frequencies in the main small mammal host species. CAA, Ctenophthalmus apertus apertus; CAG, Ctenophthalmus apertus gilcolladoi; CB, Ctenophthalmus baeticus; NF, Nosopsyllus fasciatus; LT, Leptopsylla taschenbergi; RB, Rhadinopsylla beillardae. * Sample size too small (n = 1).

Resumen del trabajo presentado al XIV Congreso de la Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM), celebrado en Jaca (Huesca) del 5 al 8 de diciembre de 2019.

Resumen del trabajo presentado al XIV Congreso de la Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM), celebrado en Jaca (Huesca) del 5 al 8 de diciembre de 2019.

Resumen del trabajo presentado a la 9th International Conference on Tularemia, celebrada en Montréal (Canada) del 16 al 19 de octubre de 2018., [Background and aim]: Tularemia is caused by the gram-negative intracellular pathogen Francisella tularensis. In Europe, the region of Castilla y León, Northwest Spain, is a major hotspot for tularemia, where the largest outbreaks of the disease have been recently reported. While rodents and lagomorphs are recognised as the main mammalian hosts in Europe, the common voles (Microtus arvalis) are documented key agents for human tularemia in Northwestern Spain, as evidenced by a spatial and temporal coincidence between human cases and increases in vole abundance. This study aimed to perform comparative genomics of F. tularensis isolates from tissue samples of F. tularensis positive voles with 11 human isolates from 2014, when an increased number of human cases was observed in the same area of Spain. [Material and Methods]: For this study, we selected thirty-four trapped voles, sampled in 80 km2 of farmland in Palencia Province, Spain (42°1′N, 4°42′W), that tested Ft-positive, by conventional PCR and hybridization by reverse line blotting (targeting lpnA), and the multi-target TaqMan PCR, tul4 and ISFtu2 assays. Tissues (liver, spleen and lung) from each animal were minced, inoculated in chocolate agar PolyViteXTM at 37°C in 5% CO2, and observed at 24, 48 and 72h post-inoculation. So far, after DNA extraction, four isolates, showing typical Ft growth, were subjected to paired-end whole-genome sequencing in an Illumina MiSeq apparatus, followed by genome assembly and bioinformatics analysis. [Results and conclusions]: All trapped voles tested positive for F. tularensis subsp. holarctica. A preliminary core-genome SNPs-based analysis, representing >99% of the genome, showed that all isolates (N=15) were distinguishable by 33 single nucleotide variant sites, representing two clear phylogenetic clusters. Noteworthy, four newly sequenced vole-isolated strains segregated together with five human-associated strains from 2014, suggesting the potential persistence of this strain in this region.

Resumen del trabajo presentado a la 9th International Conference on Tularemia, celebrada en Montréal (Canada) del 16 al 19 de octubre de 2018., [Background and aim]: Tularemia is a zoonosis caused by Francisella tularensis, a pathogen that can use a variety of transmission routes in nature as well as in humans. Since 1997 more than 1,000 human cases of tularemia have been declared in Spain in two major outbreaks, but knowledge about the epidemiology of this infection is very limited. The ability of F. tularensis to find mechanisms to persist in the environment and cause new outbreaks makes it necessary to identify, among others, the potential reservoirs during inter-epizootic periods, the main objective of this study. [Material and methods]: The sampling points were located in an area of Castilla y León, well known as “hot spots” for tularemia. They corresponded to surface water and sediments, as well as crayfish, mosquitoes, hares and ticks. Specifically, 8 zones divided into 4 subzones were sampled, including three rivers, three irrigation channels and three lagunes. Samples were collected in July and November of 2016 and 2017. For detection of Francisella lpnA was amplified by conventional PCR and hybridization by reverse line blotting with specific probes. Positive samples were confirmed by a real-time multitarget TaqMan PCR, using tul4 and ISFtu2 assays. For additional characterization sdhA gen and VNTR Ft-M19 were amplified and sequenced. [Results]: A total of 102 samples of water, 111 sediments, 343 crayfish, 156 mosquitos, 64 hares and 126 ticks from 14 hares were collected. Overall, 2 samples of water, 3 of sediments, 7 hares and 17 ticks tested positive for Francisella. Interestingly, F. tularensis subspecie holarctica was detected in water, hares and ticks while F. hispaniensis was the species detected in water and sediments. [Conclusions]: In this study we provide evidence of Francisella presence in nature during periods in which no large outbreaks of tularemia occur, and suggest that hares and ticks play an important role in the maintenance of the bacteria in the terrestrial environment. Moreover, to the best of our knowledge this is the first description of F. hispaniensis in abiotic environment, which enforces the need to assess the risk for the population and establish the necessary measures for its prevention and control.

Resumen del trabajo presentado al 3rd International Congress on Parasites of Wildlife, celebrado en Kruger National Park (South Africa) del 24 al 27 de septiembre de 2017., By experimentally adding or removing parasites, it has been shown that macro-parasites may regulate populations of their hosts. At an individual level, ecto-parasites can affect body condition, growth, life span, energy expenditure, litter size, foraging, and juvenile survival of hosts, which could translate into effects on host population abundances. We investigated the effect of a flea community (Cenophthalmus apertus, Nosopsyllus fasciatus, Leptopsylla taschenbergi) on free-living common vole (Microtus arvalis) populations from agricultural landscapes of NW Spain, where voles regularly fluctuate in numbers. We evaluated the numerical response of fleas to vole abundance (direct vs. delayed density-dependence, DD), also considering the abundance of alternative rodent hosts. We tested for negative associations between vole population growth rates (PGR) in spring, summer and winter and species-specific flea abundances. Finally, we investigated whether the body condition of voles (mass relative to size) and the reproductive effort of females (number of embryos) co-varied with flea abundance. We found that: flea abundance had a delayed DD pattern, increasing with previous (8 month before) vole abundance; at population level, a greater flea abundance was associated with a reduced vole PGR in summer and winter; and male body condition in spring and winter and the number of embryos per pregnant female were negatively associated with individual-level flea abundance. These effects varied depending on the flea species, but support the hypothesis that fleas have a regulating influence on common vole populations and have a destabilizing effect in the studied system. Experiments are required to confirm these findings.

Resumen del trabajo presentado al 15th Rodens et Spatium: International Conference on Rodent Biology, celebrada en Olomouc (Czech Republic) del 25 al 29 de julio de 2016., In many European regions, most microtine rodents exhibit multi-annual fluctuations in abundance and can cause significant crop damage and economical losses when they are overabundant during population outbreaks. In addition, they can be reservoirs of multiple pathogens responsible of serious zoonotic diseases to humans and livestock. Therefore, understanding the relationships between rodents and their pathogens under a dynamic perspective (density-dependent patterns of prevalence) may be particularly relevant in terms of effective public health management. In NW Spain, the outbreaking common vole (Microtus arvalis) recently colonized intensive agricultural landscapes where it has been pointed as a main amplification and spill-over host of Francisella tularensis (the etiological agent of tularemia). However, the epidemiological role of these fluctuating vole populations with regard to zoonotic diseases remains largely unknown. Here we describe for the first time the patterns of prevalence of F. tularensis along a complete fluctuation in abundance in a wild common vole population. Voles were captured seasonally (March, July and November) during a population outbreak between 2013 and 2015 and were screened for the occurrence of the pathogen. From a total of 243 captured voles, 46 individuals were infected, but prevalence greatly varied in time (range from 0 to 30%).We found a strong effect of vole abundance on tularemia prevalence, in a direct positive density-dependent way. We discuss the implications of the findings for our understanding of vole population regulation and public health. The increasing frequency of zoonotic disease events in rodents encourage us to go on studying the co-infection in common vole populations with other relevant pathogens.

Resumen del trabajo presentado a la 10th European Vertebrate Pest Management Conference, celebrada en Sevilla (España) del 21 al 25 de septiembre de 2015., Understanding the ecological factors that determine the population growth rate of rodent populations is fundamental in order to study population dynamics, and to predict and better manage population outbreaks. This is particularly important for species that spill over diseases or cause significant crop damages when overabundant, like common voles in NW Spain. Using six-years of seasonal (three times a year) abundance data (July 2009-March 2015), we investigated weather variables influencing local seasonal population dynamics of Microtus arvalis, Apodemus sylvaticus, Mus spretus and Crocidura russula. In that way, we used General Linear Models (GLM) to explain variation in seasonal population growth rates (PGRs) of each species with abundance and climate variables (average temperature and monthly accumulated precipitation in spring, summer, autumn and winter). Winter was the most critical period for all species, as winter temperature positively influenced winter PGR. Moreover, winter temperature positively influenced spring PGR in M. arvalis and C. russula, suggesting that warmer winters benefited vole and shrew population growth during both winter and spring. On the other hand, precipitation was crucial for summer PGR in common vole, shrew and wood mouse, while winter precipitation influenced spring PGR in M. spretus. We discuss species-specific traits (e.g. diet, size and metabolism…) that can explain how climate affects population dynamics. These results allow a better understanding of how weather affects the local population dynamics of small mammals in a typical community of Mediterranean farmlands in south-western Europe.

Resumen del trabajo presentado a la 10th European Vertebrate Pest Management Conference, celebrada en Sevilla (España) del 21 al 25 de septiembre de 2015., Biological control of rodents based on the management of raptor populations could aid to prevent or reduce agricultural damage by rodents, and therefore minimize the use of rodenticides. Recurrent common vole population outbreaks have been occurring in NW Spain during the last 40 years. These outbreaks have led to large-scale application of anticoagulant rodenticides. Since 2009, looking for a potential alternative to rodenticides, we installed a total of 300 nest-boxes over poles in three experimental areas of 2000 ha. Three nearby areas of similar extension and habitat were considered as control areas. Vole abundances were monitored three times yearly (late winter, summer and autumn) as well as the abundance of raptors, which was monitored by conducting kilometer index of abundance (KIA). The use of nest-boxes and breeding parameters for kestrels and barn owls were also recorded yearly. During the study period, a large-scale vole outbreak occurred in 2013-2014 and a lesser population peak occurred during 2011. In the treatment areas, the supplementation of nest-boxes significantly increased the abundance of kestrels, especially during summer, and also increased buzzard abundance during winter. Vole abundance was lower or more stable in the experimental areas as compared with control areas during 2011, but differences were not detectable during the 2014 outbreak in two study areas. Overall, biological control by raptors may help to control vole densities in agricultural land but may require aditional actions on large-scale vole outbreak years (increasing nest-box density, the size of the treatment area or using complementary environmentally friendly techniques).

Resumen del trabajo presentado a la 10th European Vertebrate Pest Management Conference, celebrada en Sevilla (España) del 21 al 25 de septiembre de 2015.-- et al., Nest-box installation to increase raptor numbers is an environmentally friendly technique to prevent vole plagues in agricultural systems that may help to reduce the dangerous use of anticoagulants. However, the high abundance of raptors may produce undesired effects on other non-target species of economic interest. Nest box installation on poles since 2009 increased population numbers of common kestrels Falco tinnunculus in our study agricultural areas, but also increased numbers of common buzzards Buteo buteo as they use poles as perches for hunting. We studied the effect of this raptor increase on the abundance of the red-legged partridge Alectoris rufa, a gamebird species of great socioeconomic interest in the Iberian Peninsula. For this purpose the abundance of kestrels, buzzards and partridges were monitored during five years by road surveys three times each year (April, July and November), in six agricultural areas of similar size (2000 ha each) and with (nest-box areas) and without (control areas) nest box installation. The three nest-box areas counted with 100 kestrel nest-boxes placed on poles. Our results showed that kestrel and buzzard number increases seems to have a negative effect during spring time on partridge abundances. However, a positive effect of raptor increase on partridge abundance was observed during summer time with no obvious effects on partridge abundances during winter. We suggest that partridges tend to avoid the high density of predators during the breeding season while just after breeding (July), higher densities of non partridge-specialist predators might provide protection to partridges against larger size raptors.

Resumen del trabajo presentado al XII Congreso de la Sociedad Española para la Conservación y Estudio de los Mamíferos, celebrado en Burgos del 4 al 7 de diciembre de 2015., Los parásitos pueden afectar negativamente a la reproducción y supervivencia de los hospedadores y, por lo tanto, influir sobre la dinámica de sus poblaciones. Conocer el posible papel regulador de los parásitos en la dinámica poblacional de un hospedador es particularmente importante cuando se trata de una especie que causa daños agrícolas, o afecta a la salud pública (zoonosis). Este es el caso del topillo campesino (Microtus arvalis) en los ecosistemas agrarios de Castilla y León, donde su densidad poblacional fluctúa entre años y ocasiona episodios de plaga. En este estudio evaluamos la respuesta numérica de los topillos (cambios de abundancia) frente a las variaciones de la carga de ectoparásitos (número de pulgas por hospedador), teniendo en cuenta la abundancia local de otras especies hospedadoras (Apodemus sylvaticus y Mus spretus). El estudio se centró en las tres especies principales de pulgas (Ctenophthalmus sp., Nosopsyllus fasciatus y Leptopsylla taschenbergi) identificadas en los roedores (99.67%). Por último, estudiamos las variaciones estacionales en la tasa de crecimiento poblacional (PGR) del topillo campesino y su relación con la carga parasitaria de los individuos. Los resultados indican que la carga parasitaria es menor cuando la abundancia de topillos en mayor (posible efecto de “dilución”), pero es mayor 8 meses después de altas abundancias de topillos (relación de densodependencia retrasada que puede tener un efecto regulador). A nivel de especie, únicamente la abundancia de Ctenophthalmus sp. dependió de la abundancia de M. arvalis (denso-dependencia directa y retrasada), mientras que las otras especies de pulgas dependieron fundamentalmente de la abundancia de otros hospedadores (A. sylvaticus y M. spretus). En cuanto a la influencia de los ectoparásitos sobre la PGR, los resultados indican que el incremento poblacional de topillos en verano e invierno está negativamente relacionado tanto con la abundancia de éstos como de pulgas, existiendo diferencias de tal efecto entre las distintas especies de pulgas. Estos resultados indican que las pulgas podrían jugar un papel regulador en la dinámica poblacional de los topillos.

Resumen del trabajo presentado a la 10th European Vertebrate Pest Management Conference, celebrada en Sevilla (España) del 21 al 25 de septiembre de 2015., Reproduction is the most fundamental mechanism for maintaining life over time. In Rodents reproduction rates are typically high, although temporal changes in the reproductive output of individuals are an important component of population change. In populations that periodically experience strong fluctuations in abundance, reproductive strategies and performance can change dramatically when populations are rising as compared with when are dropping down. Across the northern hemisphere, arvicoline rodents (i.e., voles and lemmings) typically show strong irruptive (often cyclic) fluctuations in abundance, which ultimately determine the maintenance of biodiversity at several trophic levels. Besides their key ecological role, some species are also considered as agricultural pests in farming environments when their numbers exceed certain abundance thresholds; such is the case of the common vole in Europe. This species has recently colonized the extensive semi-arid agricultural plains of NW Spain (Castilla-y-León region), and periodic outbreaks have followed ever since in the region. Ecological knowledge of these novel populations of farmland voles still is scarce, which jeopardizes effective sustainable management. Quantifying the temporal variation of significant biological processes, such as reproduction, is paramount in order to progress with the practical knowledge that can be use to manage vole populations. Here, we describe basic phenotypical parameters (body mass), reproductive condition (descended testes or pregnancy) and relative proportions (sex ratios) of both male and female common voles during a 6-year study (2009-2015) in intensive farmland from NW Spain. We discuss the patterns of variation found across several vole populations and contextualize their usefulness in management terms.

Resumen de la comunicación presentada en: 7th European Congress of Mammalogy - Stockholm (Sweden), August 17–21 2015, Investment in sperm numbers is a key predictor of success in sperm competition and there is usually a positive relationship between sperm competition level and male reproductive effort on ejaculates, which is often measured using relative testes size (RTS). Demographic processes can drasti- cally alter levels of sperm competition and we should expect males to respond to increasing competition risk (RTS increase with density). Here we investigate whether RTS of common voles respond to fluctuations in population density. We evaluated variation of RTS depending on current and recent densities of con- specifics, also taking into account the condition of individual males (fat levels and parasite loads). Contrary to our prediction and in line with recent findings reporting ambiguous results among other vole species, we found a reversed relationship between RTS and density. Our data show that demographic factors can strongly affect RTS and we discuss possible mechanisms to explain these findings.

Resumen del trabajo presentado al XII Congreso de la Sociedad Española para la Conservación y Estudio de los Mamíferos, celebrado en Burgos del 4 al 7 de diciembre de 2015., La agricultura intensiva es uno de los principales factores causales del “cambio global”, incluyendo transformaciones en el funcionamiento de ecosistemas y pérdidas significativas de biodiversidad. Actualmente los paisajes agrarios constituyen uno de los principales biomas del planeta, y es precisamente en éstos donde se registran los cambios más profundos en comunidades nativas de flora y fauna. Algunos de estos cambios implican que especies muy competitivas expandan su rango de distribución favorecidos por cambios en el uso del suelo, desplazando y sustituyendo a taxones nativos similares (por ej. del mismo gremio ecológico). Se resumen los aspectos más relevantes de nuestra investigación sobre la reciente colonización de las regiones agrarias de la Meseta Norte por parte del topillo campesino (Microtus arvalis), centrándonos principalmente en los cambios e impactos socio-económicos, ecológicos y sanitarios que la expansión de esta especie ha generado. Desde su llegada a los paisajes cerealistas del valle del Duero a finales del siglo XX, favorecida por el incremento del regadío, las poblaciones de M. arvalis han experimentado fuertes fluctuaciones periódicas de abundancia, ocasionando importantes plagas agrícolas y generando un intenso debate social. Los daños que los incrementos de topillos ocasionan en los cultivos, el impacto ecológico que las medidas de control tienen sobre otras especies, así como el papel amplificador de enfermedades zoonóticas que tienen estas irrupciones poblacionales, son las consecuencias con mayor repercusión social y mediática del reciente cambio de distribución de la especie. Sin embargo, otros efectos menos conspicuos pero no menos importantes también han tenido lugar: la llegada de M. arvalis a la estepa cerealista se ha correlacionado con una drástica reducción de las especies endémicas de topillos ibéricos (topillos mediterráneos y lusitanos). Un análisis global de los cambios que la agricultura intensiva produce en los ecosistemas (en este caso, la implantación de nuevos cultivos de regadío en regiones semiáridas), nos permite obtener una visión más completa y realista de sus consecuencias económicas y ambientales.

Resumen del trabajo presentado al 14th Rodens et Spatium: International Conference on Rodent Biology, celebrada en Lisboa del 28 de julio al 2 de agosto de 2014., Common voles (Microtus arvalis) can be abundant in agricultural landscapes of Europe and their numbers can strongly fluctuate through time, which confers them a key ecological role for the structure and dynamics of local communities. Also, they are often declared and controlled as agricultural pests as can cause significant socio-economical and health impacts during outbreaks. Contrary to expectations from climate warming, the species has colonized the large semi-arid agricultural plains of NW Spain largely facilitated by a synchronous and rapid increase of farming surfaces with hitherto uncommon favourable habitats (alfalfa crops) and production regimes (irrigation). Ecological knowledge of the populations recently established in farmland is scarce, so quantifying the demographic impact of specific factors (environmental and intrinsic) in the temporal and spatial variation of vole abundance is paramount in order to progress with: (1) a general understanding of the causation of rodent fluctuations and (2) the practical knowledge that can be used in the management of their impacts. Here we present novel data from seasonally monitored populations regarding vole dynamics and that of their natural enemies, including aerial (raptors) and terrestrial (weasels) predators, as well as parasites (fleas). We describe how extrinsic factors involved in trophic interactions with voles (predation and parasitism) show different (direct or delay) patterns of density-dependence during the course of population fluctuations, and tentatively discuss their impact on local vole population growth.

Resumen del trabajo presentado al 14th Rodens et Spatium: International Conference on Rodent Biology, celebrada en Lisboa del 28 de julio al 2 de agosto de 2014., The intensification of agricultural landscapes is usually associated with increases in field size and reduction of natural and semi-natural habitats, particularly field margins and fallows. These habitats are crucial for small mammals, as permanent, less-altered habitats, or as corridors for dispersion. In this study, we assessed seasonal abundance patterns of the small mammal community (Microtus arvalis, Apodemus sylvaticus, Mus spretus, and Crocidura russula) in three main habitats (alfalfa, cereal and fallows), with special emphasis on abundance at various distances from field margins. We also investigated abundance according to the field margin characteristics (topography, height, width, cover, greenness). We show that small mammal abundance typically decrease from field margins towards the core of crop fields, depending on crop type (with a more pronounced margin effect in cereals independently of season). Abundance of M. arvalis, however, was slightly constant in alfalfa at all seasons, representing an optimum habitat for its distribution. For all species, the seasonal abundances were higher in the more vegetated field margins (greater vegetation height and cover). Field margin characteristics also affected the abundance of most species, depending on season. Common vole abundance was positively associated with vegetation cover in July, and with greenness in March and November. Our results highlight the importance of field margins in agricultural landscapes, not only for biodiversity conservation but also for the management of outbreaking species such as M. arvalis.