Mating system induced lags in rates of range expansion for different simulated mating systems and dispersal strategies: a modelling study.

Mismatches between current and potential species distributions are commonplace due to lags in the response of populations to changing environmental conditions. The prevailing mating system may contribute to such lags where it leads to mating failure at the range edge, but how active dispersers might mitigate these lags using social information to inform dispersal strategies warrants greater exploration. We used an individual-based model to explore how different mating systems for species that actively search for habitat can impose a filter on the ability to colonise empty, fragmented landscapes, and explored how using social information during dispersal can mitigate the lags caused by more constrained mating systems. The mate-finding requirements implemented in two-sex models consistently led to slower range expansion compared to those that were not mate limited (i.e., female only models), even when mating was polygynous. A mate-search settlement strategy reduced the proportion of unmated females at the range edge but had little impact on rate of spread. In contrast, a negative density-dependent settlement strategy resulted in much faster spread, which could be explained by a greater number of long-distance dispersal events. Our findings suggest that even low rates of mating failure at the range edge can lead to considerable lags in range expansion, though dispersal strategies that favour colonising more distant, sparsely occupied habitat patches may effectively mitigate these lags.

Relationship type affects the reliability of dispersal distance estimated using pedigree inferences in partially sampled populations: A case study involving invasive American mink in Scotland.

Estimating dispersal-a key parameter for population ecology and management-is notoriously difficult. The use of pedigree assignments, aided by likelihood-based software, has become popular to estimate dispersal rate and distance. However, the partial sampling of populations may produce false assignments. Further, it is unknown how the accuracy of assignment is affected by the genealogical relationships of individuals and is reflected by software-derived assignment probabilities. Inspired by a project managing invasive American mink (Neovison vison), we estimated individual dispersal distances using inferred pairwise relationships of culled individuals. Additionally, we simulated scenarios to investigate the accuracy of pairwise inferences. Estimates of dispersal distance varied greatly when derived from different inferred pairwise relationships, with mother-offspring relationship being the shortest (average = 21 km) and the most accurate. Pairs assigned as maternal half-siblings were inaccurate, with 64%-97% falsely assigned, implying that estimates for these relationships in the wild population were unreliable. The false assignment rate was unrelated to the software-derived assignment probabilities at high dispersal rates. Assignments were more accurate when the inferred parents were older and immigrants and when dispersal rates between subpopulations were low (1% and 2%). Using 30 instead of 15 loci increased pairwise reliability, but half-sibling assignments were still inaccurate (>59% falsely assigned). The most reliable approach when using inferred pairwise relationships in polygamous species would be not to use half-sibling relationship types. Our simulation approach provides guidance for the application of pedigree inferences under partial sampling and is applicable to other systems where pedigree assignments are used for ecological inference.

Host-parasite biology in the real world: the field voles of Kielder.

Research on the interactions between the field voles (Microtus agrestis) of Kielder Forest and their natural parasites dates back to the 1930s. These early studies were primarily concerned with understanding how parasites shape the characteristic cyclic population dynamics of their hosts. However, since the early 2000s, research on the Kielder field voles has expanded considerably and the system has now been utilized for the study of host-parasite biology across many levels, including genetics, evolutionary ecology, immunology and epidemiology. The Kielder field voles therefore represent one of the most intensely and broadly studied natural host-parasite systems, bridging theoretical and empirical approaches to better understand the biology of infectious disease in the real world. This article synthesizes the body of work published on this system and summarizes some important insights and general messages provided by the integrated and multidisciplinary study of host-parasite interactions in the natural environment.

Mycobacterium microti tuberculosis in its maintenance host, the field vole (Microtus agrestis): characterization of the disease and possible routes of transmission.

The field vole (Microtus agrestis) is a known maintenance host of Mycobacterium microti. Previous studies have shown that infected animals develop tuberculosis. However, the disease is also known in cats and is sporadically reported from humans and other mammalian species. We examined trapped field voles from an endemic area, using a range of diagnostic approaches. These confirmed that a combination of gross and histological examination with culture is most appropriate to identify the true prevalence of the disease, which was shown to be more than 13% at times when older animals that have previously been shown to be more likely to develop the disease dominate the population. The thorough pathological examination of diseased animals showed that voles generally develop systemic disease with most frequent involvement of spleen and liver, followed by skin, lymph nodes, and lungs. The morphology of the lesions was consistent with active disease, and their distribution suggested skin wounds or oral and/or aerogenic infection as the main portal of entry. The demonstration of mycobacteria in open skin lesions, airways, and salivary glands indicated bacterial shedding from the skin and with sputum and saliva. This suggests not only the environment but also direct contact and devouring as likely sources of infection.

Pulsed resources affect the timing of first breeding and lifetime reproductive success of tawny owls.

1. According to life-history theory, environmental variability and costs of reproduction account for the prevalence of delayed reproduction in many taxa. Empirical estimates of the fitness consequences of different ages at first breeding in a variable environment are few however such that the contributions of environmental and individual variability remains poorly known. 2. Our objectives were to elucidate processes that underpin variation in delayed reproduction and to assess lifetime consequences of the age of first breeding in a site-faithful predator, the tawny owl Strix aluco L. subjected to fluctuating selection linked to cyclical variation in vole density (typically 3-year cycles with low, increasing and decreasing vole densities in successive years). 3. A multistate capture-recapture model revealed that owl cohorts had strikingly different juvenile survival prospects, with estimates ranging from 0.08 to 0.33 respectively for birds born in Decrease and Increase phases of the vole cycle. This resulted in a highly skewed population structure with >75% of local recruits being reared during Increase years. In contrast, adult survival remained constant throughout a vole cycle. The probability of commencing reproduction was lower at age 1 than at older ages, and especially so for females. From age 2 onwards, pre-breeders had high probabilities of entering the breeding population. 4. Variation in lifetime reproductive success was driven by the phase of the vole cycle in which female owls started their breeding career (26-47% of variance explained, whether based on the number of local recruits or fledglings), more than by age at first breeding or by conditions experienced at birth. Females who postponed reproduction to breed for the first time at age 3 during an Increase phase, produced more recruits, even when accounting for birds that may have died before reproduction. No such effects were detected for males. 5. Sex-specific costs of early reproduction may have accounted for females being more prone to delay reproduction. Contrary to expectations from a best-of-a-bad job strategy, early-hatched, hence potentially higher-quality females were more likely to breed at age 1, but then experienced rapidly declining food resources and so seemed caught in a life-history trap set by the multiannual vole cycle.

Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations.

The importance of Ixodes ricinus in the transmission of tick-borne pathogens is well recognized in the United Kingdom and across Europe. However, the role of coexisting Ixodes species, such as the widely distributed species Ixodes trianguliceps, as alternative vectors for these pathogens has received little attention. This study aimed to assess the relative importance of I. ricinus and I. trianguliceps in the transmission of Anaplasma phagocytophilum and Babesia microti among United Kingdom field voles (Microtus agrestis), which serve as reservoir hosts for both pathogens. While all instars of I. trianguliceps feed exclusively on small mammals, I. ricinus adults feed primarily on larger hosts such as deer. The abundance of both tick species and pathogen infection prevalence in field voles were monitored at sites surrounded with fencing that excluded deer and at sites where deer were free to roam. As expected, fencing significantly reduced the larval burden of I. ricinus on field voles and the abundance of questing nymphs, but the larval burden of I. trianguliceps was not significantly affected. The prevalence of A. phagocytophilum and B. microti infections was not significantly affected by the presence of fencing, suggesting that I. trianguliceps is their principal vector. The prevalence of nymphal and adult ticks on field voles was also unaffected, indicating that relatively few non-larval I. ricinus ticks feed upon field voles. This study provides compelling evidence for the importance of I. trianguliceps in maintaining these enzootic tick-borne infections, while highlighting the potential for such infections to escape into alternative hosts via I. ricinus.

Parasite interactions in natural populations: insights from longitudinal data.

The physiological and immunological state of an animal can be influenced by current infections and infection history. Consequently, both ongoing and previous infections can affect host susceptibility to another parasite, the biology of the subsequent infection (e.g. infection length) and the impact of infection on host morbidity (pathology). In natural populations, most animals will be infected by a succession of different parasites throughout the course of their lives, with probably frequent concomitant infections. The relative timing of different infections experienced by a host (i.e. the sequence of infection events), and the effects on factors such as host susceptibility and host survival, can only be derived from longitudinal data on individual hosts. Here we review some of the evidence for the impact of co-infection on host susceptibility, infection biology and pathology focusing on insights obtained from both longitudinal studies in humans and experiments that explicitly consider the sequence of infection. We then consider the challenges posed by longitudinal infection data collected from natural populations of animals. We illustrate their usefulness using our data of microparasite infections associated with field vole (Microtus agrestis) populations to examine impacts on susceptibility and infection length. Our primary aim is to describe an analytical approach that can be used on such data to identify interactions among the parasites. The preliminary analyses presented here indicate both synergistic and antagonistic interactions between microparasites within this community and emphasise that such interactions could have significant impacts on host-parasite fitness and dynamics.

Tuberculosis (Mycobacterium microti) in wild field vole populations.

Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5.2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10.78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13.15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.

Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom?

The importance of wild rodents as reservoirs of zoonotic tick-borne pathogens is considered low in the United Kingdom because, in studies to date, those parasitized by exophilic Ixodes ricinus ticks carry almost exclusively larvae and thus have a minor role in transmission cycles. In a cross-sectional study, 11 (6.7%) of 163 field voles (Microtus agrestis) captured at field sites in Northern England were PCR-positive for Anaplasma phagocytophilum. The voles were found to act as hosts for both larval and nymphal I. ricinus and all stages of the nidicolous tick I. trianguliceps, and eight individuals were infested with ticks of both species at the same time. Two of 158 larval and one of 13 nymphal I. ricinus, as well as one of 14 larval and one of 15 nymphal I. trianguliceps collected from the rodents were PCR-positive. These findings suggest that habitats where field voles are abundant in the United Kingdom may pose a risk of A. phagocytophilum infection because (i) field voles, the most abundant terrestrial mammal in the United Kingdom, may be a competent reservoir; (ii) the field voles are hosts for both nymphal and larval ixodid ticks so they could support endemic cycles of A. phagocytophilum; and (iii) they are hosts for nidicolous I. trianguliceps, which may alone maintain endemic cycles, and exophilic I. ricinus ticks, which could act as a bridge vector and transmit infections to humans and domesticated animals.

The compensatory potential of increased immigration following intensive American mink population control is diluted by male-biased dispersal.

Attempts to mitigate the impact of invasive species on native ecosystems increasingly target large land masses where control, rather than eradication, is the management objective. Depressing numbers of invasive species to a level where their impact on native biodiversity is tolerable requires overcoming the impact of compensatory immigration from non-controlled portions of the landscape. Because of the expected scale-dependency of dispersal, the overall size of invasive species management areas relative to the dispersal ability of the controlled species will determine the size of any effectively conserved core area unaffected by immigration from surrounding areas. However, when dispersal is male-biased, as in many mammalian invasive carnivores, males may be overrepresented amongst immigrants, reducing the potential growth rate of invasive species populations in re-invaded areas. Using data collected from a project that gradually imposed spatially comprehensive control on invasive American mink (Neovison vison) over a 10,000 km2 area of NE Scotland, we show that mink captures were reduced to almost zero in 3 years, whilst there was a threefold increase in the proportion of male immigrants. Dispersal was often long distance and linking adjacent river catchments, asymptoting at 38 and 31 km for males and females respectively. Breeding and dispersal were spatially heterogeneous, with 40 % of river sections accounting for most captures of juvenile (85 %), adult female (65 %) and immigrant (57 %) mink. Concentrating control effort on such areas, so as to turn them into "attractive dispersal sinks" could make a disproportionate contribution to the management of recurrent re-invasion of mainland invasive species management areas.

Matrilineal genetic structure and female-mediated gene flow in red grouse (Lagopus lagopus scoticus): an analysis using mitochondrial DNA.

DNA sequence variation at the hypervariable 5' end of the mitochondrial control region was examined in 247 individuals to detect genetic divergence among 14 populations of red grouse (Lagopus lagopus scoticus) in northeastern Scotland. Ten haplotypes were resolved, several of which were shared among populations. Analysis of molecular variance, Nei's gamma ST, and a cladistic estimate of the amount of gene flow indicated a lack of overall population differentiation. Patterns of overall panmixia are in stark contrast to previous reports of localized subdivision among the same set of populations detected using hypervariable microsatellite markers. Because grouse cocks are territorial and show extreme natal philopatry and females are the dispersing sex, such discordance could be explained by sex-biased dispersal, with extensive female-mediated gene flow preventing mitochondrial DNA divergence. However, it is difficult to reconcile how effective dispersal of females would not homogenize both mitochondrial and nuclear structure simultaneously. We use a model that examines the spatial and temporal dynamics of diparentally and uniparentally inherited genes to show that, under realistic ecological scenarios and with specific differences in the dispersal of males and females, the local effective size of the nuclear genome can be less than that of the mitochondrial and the patterns of structuring we observe are meaningful.

Generation of periodic waves by landscape features in cyclic predator-prey systems.

The vast majority of models for spatial dynamics of natural populations assume a homogeneous physical environment. However, in practice, dispersing organisms may encounter landscape features that significantly inhibit their movement. We use mathematical modelling to investigate the effect of such landscape features on cyclic predator-prey populations. We show that when appropriate boundary conditions are applied at the edge of the obstacle, a pattern of periodic travelling waves develops, moving out and away from the obstacle. Depending on the assumptions of the model, these waves can take the form of roughly circular 'target patterns' or spirals. This is, to our knowledge, a new mechanism for periodic-wave generation in ecological systems and our results suggest that it may apply quite generally not only to cyclic predator-prey interactions, but also to populations that oscillate for other reasons. In particular, we suggest that it may provide an explanation for the observed pattern of travelling waves in the densities of field voles (Microtus agrestis) in Kielder Forest (Scotland-England border) and of red grouse (Lagopus lagopus scoticus) on Kerloch Moor (northeast Scotland), which in both cases move orthogonally to any large-scale obstacles to movement. Moreover, given that such obstacles to movement are the rule rather than the exception in real-world environments, our results suggest that complex spatio-temporal patterns such as periodic travelling waves are likely to be much more common in the natural world than has previously been assumed.

Spatial asynchrony and periodic travelling waves in cyclic populations of field voles.

We demonstrate evidence for the presence of travelling waves in a cyclic population of field voles in northern Britain by fitting simple, empirical models to spatially referenced time series data. Population cycles were broadly synchronous at all sites, but use of Mantel correlations suggested a strong spatial pattern along one axis at a projection line 72 degrees from North. We then fitted a generalized additive model to log population density assuming a fixed-form travelling wave in one spatial dimension for which the density at each site was offset in time by a constant amount from a standard density-time curve. We assumed that the magnitude of this offset would be proportional to the spatial separation between any given site and the centroid of the sampling sites, where separation is the distance between sites in a fixed direction. After fitting this model, we estimated that the wave moved at an average speed of 19 km yr-1, heading from West to East at an angle of 78 degrees from North. Nomadic avian predators which could synchronize populations over large areas are scarce and the travelling wave may be caused by density-dependent dispersal by field voles and/or predation by weasels, both of which act at a suitably small spatial scale.

Host-parasite interactions in a fragmented landscape.

Theory suggests that habitat fragmentation should reduce the risk of being parasitised due to reduced size and increased isolation of the host population. It is predicted that a threshold host population size exists, below which parasites will not be able to persist. Small mammals were trapped and their ecto-parasites removed in 14 field margins of varying widths over 2 years in a highly fragmented agro-ecosystem. No evidence to suggest the presence of a threshold in parasite prevalence was found, which may be due to the high rate of host movement and transiency within the system. Contrary to expectation, the probability of infestation decreased with host abundance and the abundance of alternative hosts, suggesting a dilution effect. The relatively long life cycle of small mammal specialist tick and flea species present under the prevailing environmental conditions may have left the parasites unable to keep up with the rate of reproduction and dispersal of the host. It is important to consider changes in the behaviour of the host and the presence of alternative hosts when predicting the effects of habitat fragmentation on disease spread.

Are silica defences in grasses driving vole population cycles?

Understanding the factors that drive species population dynamics is fundamental to biology. Cyclic populations of microtine rodents have been the most intensively studied to date, yet there remains great uncertainty over the mechanisms determining the dynamics of most of these populations. For one such population, we present preliminary evidence for a novel mechanism by which herbivore-induced reductions in plant quality alter herbivore life-history parameters and subsequent population growth. We tested the effect of high silica levels on the population growth and individual performance of voles (Microtus agrestis) reared on their winter food plant (Deschampsia caespitosa). In sites where the vole population density was high, silica levels in D. caespitosa leaves collected several months later were also high and vole populations subsequently declined; in sites where the vole densities were low, levels of silica were low and population density increased. High silica levels in their food reduced vole body mass by 0.5% a day. We argue that silica-based defences in grasses may play a key role in driving vole population cycles.

Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics.

Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.

Widespread gene flow and high genetic variability in populations of water voles Arvicola terrestris in patchy habitats.

Theory predicts that the impact of gene flow on the genetic structure of populations in patchy habitats depends on its scale and the demographic attributes of demes (e.g. local colony sizes and timing of reproduction), but empirical evidence is scarce. We inferred the impact of gene flow on genetic structure among populations of water voles Arvicola terrestris that differed in average colony sizes, population turnover and degree of patchiness. Colonies typically consisted of few reproducing adults and several juveniles. Twelve polymorphic microsatellite DNA loci were examined. Levels of individual genetic variability in all areas were high (H(O) = 0.69-0.78). Assignments of juveniles to parents revealed frequent dispersal over long distances. The populations showed negative F(IS) values among juveniles, F(IS) values around zero among adults, high F(ST) values among colonies for juveniles, and moderate, often insignificant, F(ST) values for parents. We inferred that excess heterozygosity within colonies reflected the few individuals dispersing from a large area to form discrete breeding colonies. Thus pre-breeding dispersal followed by rapid reproduction results in a seasonal increase in differentiation due to local family groups. Genetic variation was as high in low-density populations in patchy habitats as in populations in continuous habitats used for comparison. In contrast to most theoretical predictions, we found that populations living in patchy habitats can maintain high levels of genetic variability when only a few adults contribute to breeding in each colony, when the variance of reproductive success among colonies is likely to be low, and when dispersal between colonies exceeds nearest-neighbour distances.

The effects of the size and shape of landscape features on the formation of traveling waves in cyclic populations.

Recent field data indicate that in a number of cyclic populations, the cycles are organized spatially with the form of a periodic traveling wave. One way in which this type of wave is generated is when dispersing individuals encounter landscape features that impede movement in certain directions. In this article, we investigate the dependence of such periodic waves on ecological parameters and on the form of the landscape feature. Using a standard predator-prey model as a prototype for a cyclic population, we calculate the speed and amplitude of waves generated by a large landscape feature. This enables us to determine parameters for which the waves are stable; in other cases, they evolve into irregular oscillations. We then undertake for the first time a detailed study of the effects of the size and shape of a landscape feature on the waves that it generates. We show that size rather than shape is the key wave-forming property, with smaller obstacles generating waves with longer wavelength and waves from larger landscape features dominating those from smaller ones. Our results suggest that periodic traveling waves may be much more common than has previously been assumed in real ecological systems, and they enable quantitative predictions on the properties of these waves for particular cases.

Life-history traits of voles in a fluctuating population respond to the immediate environment.

Life-history traits relating to growth and reproduction vary greatly among species and populations and among individuals within populations. In vole populations, body size and age at maturation may vary considerably among locations and among years within the same location. Individuals in increasing populations are typically larger and start reproduction earlier in the spring than those in declining populations. The cause of such life-history variation within populations has been subject of much discussion. Much of the controversy concerns whether the memory of past conditions, leading to delayed effects on life-history traits, resides in the environment (for example, predators, pathogens or food) or intrinsically within populations or individuals (age distribution, physiological state, genetic or maternal effects). Here we report from an extensive field transplant experiment in which voles were moved before the breeding season between sites that differed in average overwintering body mass. Transplanted voles did not retain the characteristics of their source population, and we demonstrate an over-riding role of the immediate environment in shaping life-history traits of small rodents.

Spatial population dynamics: analyzing patterns and processes of population synchrony.

The search for mechanisms behind spatial population synchrony is currently a major issue in population ecology. Theoretical studies highlight how synchronizing mechanisms such as dispersal, regionally correlated climatic variables and mobile enemies might interact with local dynamics to produce different patterns of spatial covariance. Specialized statistical methods, applied to large-scale survey data, aid in testing the theoretical predictions with empirical estimates. Observational studies and experiments on the demography of local populations are paramount to identify the true ecological mechanisms. The recent achievements illustrate the power of combining theory, observation and/or experimentation and statistical modeling in the ecological research protocol.