Juan José Luque-Larena

• Ph.D. Universitat de Barcelona (UB)
• Professor (Full) at University of Valladolid

The study of rodent population cycles has greatly contributed, both theoretically and empirically, to our understanding of the circumstances under which predator–prey interactions destabilize populations. According to the specialist predator hypothesis, reciprocal interactions between voles and small predators that specialize on voles, such as weas...

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate ov...

We screened 526 wild small mammals for zoonotic viruses in northwest Spain and found hantavirus in common voles (Microtus arvalis) (1.5%) and high prevalence (48%) of orthopoxvirus among western Mediterranean mice (Mus spretus). We also detected arenavirus among small mammals. These findings suggest novel risks for viral transmission in the region.

The dynamics of cyclic populations distributed in space result from the relative strength of synchronising influences and the limited dispersal of destabilising factors (activators and inhibitors), known to cause multi‐annual population cycles. However, while each of these have been well studied in isolation, there is limited empirical evidence of...

Iberian hare populations have suffered severe declines during recent decades in Spain. Between 1970 and 1990s, a rapid increase in irrigation crop surface in NW Spain (Castilla-y-León region) was followed by a common vole massive range expansion and complete colonization of lowland irrigated agricultural landscapes from mountainous habitats. The su...

Increasing abundance of large ungulates is raising human-wildlife impacts and the effectiveness of recreational hunting to reduce their population growth is increasingly questioned. We report on long-term trends (> 15 years) in wildlife-vehicle collisions (WVC) and hunting bags, and on associations between the annual growth rate of WVC and that of...

Francisella tularensis is the pathogen of tularemia, a zoonotic disease that have a broad range of hosts. Its epidemiology is related to aquatic environments, particularly in the subspecies holarctica. In this review, we explore the role of water and mosquitoes in the epidemiology of Francisella in Europe. F. tularensis epidemiology has been linked...

BACKGROUND The common vole has invaded the agroecosystems of northwestern Spain, where outbreaks cause important crop damage and management costs. Little is yet known about the factors causing or modulating vole fluctuations. Here, we used 11 years of vole abundance monitoring data in 40 sites to study density‐dependence and weather influence on vo...

Introduction Francisella tularensis is a highly infectious bacterium that causes the zoonotic disease tularemia. The development of genotyping methods, especially those based on whole-genome sequencing (WGS), has recently increased the knowledge on the epidemiology of this disease. However, due to the difficulties associated with the growth and iso...

Rodent populations often undergo large, regular fluctuations. We studied immunological condition and physiological stress in the common vole and how it varied with environmental factors linked with population fluctuations, namely flea and Francisella tularensis (the bacterium causing tularemia) prevalence. We used two leukocyte indices, neutrophil-...

The common vole (Microtus arvalis Pallas) is considered one of the most harmful pests for agriculture in Europe, since its natural cyclical outbreaks are linked to risk situations that can lead to significant crop losses. Furthermore, it can also constitute a public health problem as a potential environmental amplifier of zoonotic diseases, some of...

The dynamics of cyclic populations distributed in space result from the relative strength of synchronising influences and the limited dispersal of destabilising factors (activators and inhibitors), known to cause multi-annual population cycles. However, while each of these have been well studied in isolation, there is limited empirical evidence abo...

The expansion and intensification of agriculture are driving profound changes in ecosystems worldwide, favoring the (re)emergence of many human infectious diseases. Muroid rodents are a key host group for zoonotic infectious pathogens and frequently invade farming environments, promoting disease transmission and spillover. Understanding the role th...

Authors would like to correct error in affiliation in the original publication of the article.

Background Fleas frequently infest small mammals and play important vectoring roles in the epidemiology of (re)emerging zoonotic disease. Rodent outbreaks in intensified agro-ecosystems of North-West Spain have been recently linked to periodic zoonotic diseases spillover to local human populations. Obtaining qualitative and quantitative information...

Background: Fleas frequently infest small mammals and play important vectoring roles in the epidemiology of (re)emerging zoonotic disease. Rodent outbreaks in intensified agroecosystems of NW Spain have been recently linked to periodic zoonotic disease spillover to local human populations. Obtaining qualitative and quantitative information about th...

Background Fleas frequently infest small mammals and play important vectoring roles in the epidemiology of (re)emerging zoonotic disease. Rodent outbreaks in intensified agro-ecosystems of NW Spain have been recently linked to periodic zoonotic disease spillover to local human populations. Obtaining qualitative and quantitative information about th...

Background: Fleas frequently infest small mammals and play important vectoring roles in the epidemiology of (re)emerging zoonotic disease. Rodent outbreaks in intensified agro-ecosystems of NW Spain have been recently linked to periodic zoonotic disease spillover to local human populations. Obtaining qualitative and quantitative information about t...

Common voles (Microtus arvalis) are widespread in the European agricultural landscape from central Spain to central Russia. During population outbreaks, significant damage to a variety of crops is caused and the risk of pathogen transmission from voles to people increases. In 2019, increasing or unusually high common vole densities have been report...

Small mustelids such as weasels are highly specialized predators of small rodents. Their diminutive size allows hunting for prey underground, but also means that they are bite-sized predators, preyed upon by other larger predators. Habitat use by weasels is therefore expected to depend not only on prey abundance, but also on predation risk. We repo...

Weasels are bite-sized predators highly specialized on small rodents and hypothesized to cause the population cycles of these prey in northern Europe. We studied the numerical response of the common weasel (Mustela nivalis) to fluctuating abundances of common voles (Microtus arvalis) in southern Europe. We show that both predator and prey exhibited...

We detected Francisella tularensis and Bartonella spp. in fleas parasitizing common voles (Microtus arvalis) northwestern Spain; mean prevalences were 6.1% and 51%, respectively. Contrasted vector–host associations in the prevalence of these bacteria suggest that fleas have distinct roles in the transmission cycles of each pathogen in nature.

Diseases and host dynamics are linked, but their associations may vary in strength, be time lagged, and depend on environmental influences. Where a vector is involved in disease transmission, its dynamics are an additional influence, and we often lack a general understanding on how diseases, hosts and vectors interact. We report on the occurrence o...

Common voles are a main European facultative, fossorial, farmland rodent pest that can greatly reduce crop yields during population outbreaks. Crop protection against common voles is a complex task that requires the consideration of a set of preventive and control measures within an integrated pest management strategy. A possible option could be to...

This RData file contains all the objects needed for fitting Bayesian Spatial Capture-Recapture models using R and Nimble (June) from the article: Romairone, J., Jimenez, J., Luque-Larena, J. J., & Mougeot, F. (2018). Spatial capture-recapture design and modelling for the study of small mammals. PLoS One, 13(6), e0198766. If any technical advice is...

This RData file contains all the objects needed for fitting Bayesian Spatial Capture-Recapture models using R and Nimble (May) from the article: Romairone, J., Jimenez, J., Luque-Larena, J. J., & Mougeot, F. (2018). Spatial capture-recapture design and modelling for the study of small mammals. PLoS One, 13(6), e0198766. If any technical advice is n...

Spatial capture-recapture modelling (SCR) is a powerful analytical tool to estimate density and derive information on space use and behaviour of elusive animals. Yet, SCR has been seldom applied to the study of ecologically keystone small mammals. Here we highlight its potential and requirements with a case study on common voles (Microtus arvalis)....

R script and model outputs for May. (HTML)

R script and model outputs for June. (HTML)

Bai et al. (2018) determined that China's increasing milk demand is expected to raise global greenhouse gas (GHG) emissions by 35%, expand dairy land by 32% and lift nitrogen pollution by 48%. Producing the additional milk in China adds to the environmental cost of animal feed transfers (from 1 to 6.2 Tg of alfalfa), while importing the extra milk...

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 abundanc...

Tularemia in humans in northwestern Spain is associated with increases in vole populations. Prevalence of infection with Francisella tularensis in common voles increased to 33% during a vole population fluctuation. This finding confirms that voles are spillover agents for zoonotic outbreaks. Ecologic interactions associated with tularemia preventio...

Las poblaciones de algunos herbívoros silvestres que presentan dinámicas inestables (irrupciones multianuales de abundancia, de carácter cíclico o no), constituyen un fenómeno natural de amplio interés para la Ecología. Durante casi un siglo el estudio de los mecanismos causales que subyacen en este tipo de pululaciones poblacionales ha atraído la...

Small rodents are common inhabitants of farmlands where they play key ecosystem roles but can also be major pests when overabundant, causing crop damages and significant economic losses. Agricultural landscapes are characterised by high fragmentation with remnant semi-natural habitats being typically restricted to narrow field margins. These linear...

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, und...

doi: 10.1016/j.agee.2016.06.041

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 an...

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 i...

During last decades, large tularemia outbreaks in humans have coincided in time and space with population outbreaks of common voles in North-western Spain, leading us to hypothesize that this rodent species acts as a key spillover agent of Francisella tularensis in the region. Here, we evaluate for the first time a potential link between irruptive...

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 expe...

Sperm viability, acrosome integrity, motility, and swimming velocity are determinants of male fertility and exhibit an extreme degree of variation among closely related species. Many of these sperm parameters are associated with sperm ATP content, which has led to predictions of tradeoffs between ATP content and sperm motility and velocity. Selecti...

The common vole, considered a rodent pest when overabundant in agricultural areas, was traditionally absent from the agricultural plains of Castilla-y-León, NW Spain. However, it rapidly invaded ca. 50.000 km2 of agricultural land, where regular outbreaks have caused crop damages and conflict with farmers. To better understand the factors that trig...

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...

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 hea...

Sexual selection may promote divergence between populations. Sperm competition, one form of post-copulatory sexual selection, is known to favour changes in ejaculate quality and sperm swimming speed, which improve ejaculate competitiveness. We thus tested the prediction that natural populations from species with high levels of sperm competition sho...

By the end of last century the distribution range of Microtus arvalis in NW Spain greatly expanded to encompass agricultural lowlands (ca. 5 million ha), followed by the appearance of regular crop-damaging population outbreaks. We investigated plausible causal factors and found a strong association between an increase in irrigated crop surface and...

Irruptive populations of rodents cause damage to agriculture worldwide. By the end of the last century, the distribution rangeof Microtus arvalis in NW Spain greatly expanded to encompass agricultural habitats, with the appearance of crop damagingpopulation outbreaks. The absence of long term vole monitoring data has so far precluded outbreak forec...

BACKGROUND: Ecologically based rodent pest management using biological control has never been evaluated for vole plagues in Europe, although it has been successfully tested in other systems. The authors report on the first large-scale replicated experiment to study the usefulness of nest-box installation for increasing the breeding density of commo...

We describe novel aspects of the social organisation of the Pyrenean desman, Galemys pyrenaicus, by studying home range and shelter use behaviour in a local population. A total of 45 individuals were trapped of which 20 provided informative radiotracking data. In contrast to the currently accepted hypothesis [Stone RD. The social organization of th...

PAML codeml clade analysis. Models and analysis employed to detect the mode of selection acting on Protamine 1 and Protamine 2 domains. The employed models were compared by means of Likelihood-ratio-tests. (TIFF)

Amino acid sequence alignment of cleaved-Protamine 2 Study species (Cricetidae) represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetulus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Mi...

Amino acid sequence alignment of mature-Protamine 2. Study species (Cricetidae) represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetulus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Mi...

Codeml output file (M2) for mature-Protamine 2. Included species of Cricetidae represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetelus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Mic...

Phylogenetic trees. A - Tree of study species (Cricetidae). Input tree for branch and site analyses. Mus m. musculus was used as outgroup. B - Tree of study species (Cricetidae) including 12 rodent species as a background. Oryctolagus cuniculus was used as an outgroup. Input tree for clade analyses. Phylogenetic trees were constructed based on lite...

Amino acid sequence alignment of Protamine 1. Study species (Cricetidae) represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetulus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Microtus...

Codeml output file (M2) for Protamine 1. Included species of Cricetidae represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetelus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Microtus g...

Codeml output file (M2) for cleaved-Protamine 2. Included species of Cricetidae represented by abbreviated code: Arvicola sadipus (ASA), Arvicola terrestris (ATE), Clethrionomys glareolus (CGL), Cricetelus griseus (CGR), Chionomys nivalis (CNI), Microtus agrestis (MAG), Microtus arvalis (MAR), Mesocricetus auratus (MAU), Microtus cabrerae (MCA), Mi...

Sexual selection has been proposed as the driving force promoting the rapid evolutionary changes observed in some reproductive genes including protamines. We test this hypothesis in a group of rodents which show marked differences in the intensity of sexual selection. Levels of sperm competition were not associated with the evolutionary rates of pr...

By the end of last century the distribution range of Microtus arvalis in NW Spain greatly expanded and outbreaks began to be reported in recently-colonised agricultural habitats. Ever since, novel impacts to regional farming, biodiversity conservation and public health have recurrently been associated to vole outbreaks. Here we present the first at...

it has never been evaluated for cyclic vole plagues in Europe. We report the first large-scale replicated experiment to study the usefulness of artificially increasing populations of Common kestrels (Falco tinnunculus) and Barn owls (Tyto alba) to control common vole populations in agricultural habitats where nesting sites for raptors are scarce. T...

Sperm competition favours an increase in sperm swimming velocity that maximises the chances that sperm will reach the ova before rival sperm and fertilise. Comparative studies have shown that the increase in sperm swimming speed is associated with an increase in total sperm size. However, it is not known which are the first evolutionary steps that...

Reconstructed phylogenetic tree of the muroid species used in this study. The tree was constructed based on the literature and on the analysis of cytochrome b sequences Details are given in the Materials and Methods section. (TIF)

Species collection localities. Numbers indicate species as follows: 1, Arvicola terrestris (Spain); 2, Chionomys nivalis (Spain); 3, Clethrionomys glareolus (Spain); 4, Microtus arvalis (Spain); 5, Microtus cabrerae (Spain); 6, Microtus duodecimcostatus (Spain); 7, Microtus lusitanicus (Spain); 8, Apodemus sylvaticus (Spain); 9, Mus cookii (Thailan...

Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact...

Many studies show that prey should not flee immediately from approaching predators, but should adjust their fleeing distance to minimize flight costs. We explored a new scenario where an ambush predator appears close to a relatively cryptic prey, that the predator has not yet detected. Then, instead of approaching further, the predator stops and st...

A common vole (Microtus arvalis) population peak in Northern Spain in 2007 was treated with large scale application of chlorophacinone, an anticoagulant rodenticide of the indandione family. Voles found dead and trapped alive were collected in treated and untreated areas. Residues of chlorophacinone were analyzed in liver of voles by HPLC-UV. Also,...

Habitat heterogeneity is predicted to profoundly influence the dynamics of indirect interspecific interactions; however, despite potentially significant consequences for multi-species persistence, this remains almost completely unexplored in large-scale natural landscapes. Moreover, how spatial habitat heterogeneity affects the persistence of inter...

The conservation problems affecting the endangered rodent Microtus cabrerae are mainly related to habitat loss and fragmentation. In the present study, we examined the presence/absence of the species in a group of potentially suitable habitat patches, and then evaluated the microhabitat attributes of locations used by wild-ranging individuals withi...

DESCRIPCIÓN Es un arvicolino de tamaño pequeño/mediano (hasta 30 g). Medidas corporales, CC: 90,0-120,0 mm; C: 40,0-60,0 mm; P: 17,0-20,0 mm; O: 11,0-15,0 mm; Ps: 14,0-30,0 g. Una característica diferen-cial es el color rojizo del dorso que muestran los adultos. El pelaje es claramente bicolor, con el dorso castaño rojizo que se degrada por los fla...

DESCRIPCIÓN Es un arvicolino de tamaño mediano y de aspecto robusto. Hocico bastante romo y cola relativamente corta. Aunque las orejas están más cubiertas por el pelo, externamente presenta una morfología muy similar a la del topillo campesino, Microtus arvalis, del que puede llegar a ser difícil de distinguir. Medidas corporales, CC: 95,0-123,0 m...

When confronted with a predator, prey are often in close proximity to conspecifics. This situation has generated several hypotheses regarding antipredator strategies adopted by individuals within groups of gregarious species, such as the "risk dilution," "early detection," or "collective detection" effects. However, whether short-term temporary agg...

Theoretical models and empirical evidence suggest that prey should not flee immediately upon detecting an approaching predator, but instead should adjust their escape response to minimize the costs of flight. Similarly, after deciding to escape, animals should tend to adjust the magnitude and characteristics of their escape response according to th...

Adaptive models predict that variation in the spacing of microtines during reproductive periods may reflect mating strategies linked to differences in habitat characteristics. Using spatial and morphological analyses, we aimed to assess the mating system adopted by a population of rock-dwelling snow voles, Chionomys nivalis (Martins, 1842), and its...

The aim of this study was to examine how factors affecting male scent attractiveness to females interact with factors influencing male social dominance in rock-dwelling snow voles, Chionomys nivalis. We analysed the effect of particular phenotypic traits of male fitness, including relative body weight, bilateral asymmetry levels and haematocrit vol...

Among microtine rodents, reaction to chemical cues from conspecifics is assumed to reflect social and spatial relationships. Generally, strong attraction of particular odours correlates with non-aggressive behaviour and high spatial tolerance towards odour donors, whereas weak attraction correlates with greater levels of aggression and spatial segr...

We examined winter social behaviour of the snow voleChionomys nivalis Martins, 1842, a rock-dwelling microtine found principally in high-mountain biotopes. We conducted dyadic encounters among wild-caughtC. nivalis to determine patterns of intraspecific tolerance and the degree of aggressiveness between and within sexes during wintering periods. Ou...

We conducted a laboratory experiment to examine whether dominance status affects the use of locations occupied (i.e. scent-marked) by same-sex conspecifics among wild-caught snow vole males (Chionomys nivalis). Given that the costs of invading scent-marked areas should partially depend on the intruder's competitive ability, we hypothesised that, on...

Environmental conditions in mountainous regions have influenced the nature of some adaptations among small mammals and this may apply to strategies of habitat use in alpine biotopes. In the present paper, microhabitat use in relation to microhabitat availability of a population of snow voles Chionomys nivalis Martins, 1842, a nonhibernating microti...

The ‘scent-matching’ hypothesis predicts that competitors could identify resource holders by investigating scent marks from a given area and matching these with the owner's odour when they meet. Previous studies on small rodents have supported the use of scent matching among males with mutually exclusive ranges. We designed an experiment to evaluat...