Xavier Lambin

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.

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks.

The statistical aggregation of parasites among hosts is often described empirically by the negative binomial (Poisson-gamma) distribution. Alternatively, the Poisson-lognormal model can be used. This has the advantage that it can be fitted as a generalized linear mixed model, thereby quantifying the sources of aggregation in terms of both fixed and random effects. We give a worked example, assigning aggregation in the distribution of sheep ticks Ixodes ricinus on red grouse Lagopus lagopus scoticus chicks to temporal (year), spatial (altitude and location), brood and individual effects. Apparent aggregation among random individuals in random broods fell 8-fold when spatial and temporal effects had been accounted for.

Natal Philopatry, Competition for Resources, and Inbreeding Avoidance in Townsend's Voles (Microtus Townsendii)

Individuals may leave their birthsite before reproducing or they may postpone reproduction because they are at risk of engaging in inbred matings with their close relatives or because they are exposed to severe competition for resources or for mates. I studied whether avoidance of inbreeding and intrasexual competition determine the seasonal changes in the rate of philopatry and the fate of individual Townsends voles (Microtus townsendii). By marking most nestlings before weaning, I knew which recruits were related to one another and to which adult female. There was a pronounced sexual bias in the tendency to remain close to the birth site: 9% of all juvenile males and 33% of all juvenile females entered the breeding population on their natal grid. Males settled farther from their birth site than females did. The proportion of males and females reproducing on their natal grid changed markedly over the breeding season. More males and females reproduced if they were born at the beginning of the breeding season or when breeding activity was depressed by botfly infestation. Seasonal changes in female philopatry were consistent with the hypothesis that females disperse in response to competition for resources with breeding females. Females born at high adult female density were less likely to be recruited than those born at other times. They also dispersed farther at low than at high density, probably in response to habitat saturation. Avoidance of extreme inbreeding influenced the dispersal tendency of maturing males. Males were less likely to join the breeding population if their mother or a littermate sister was present in their home range when they matured than if they had no female close relatives in their home range. Males with their mother alive at sexual maturation settled farther than males whose mother had disappeared by that time. I conclude that inbreeding avoidance influenced natal philopatry in males and that competition for resources influenced natal philopatry in females.

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° 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 19km yr-1, heading from West to East at an angle of 78° 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.

Europe-Wide Dampening of Population Cycles in Keystone Herbivores

Cycling in Unison Many small mammals, especially voles, display semi-regular cycles of population boom and bust. Given the fundamental importance of small mammals as basal consumers and prey, such cycles can have cascading effects in trophic food webs. Cornulier et al. (p. 63) collated raw data from vole populations across Europe collected over the past 18 years. Reduction in winter growth rate was common across a wide variety of habitats with very different local climates, suggesting the presence of a continental-scale climatic driver of vole populations. Synchronicity in vole population fluctuation across Europe suggests a common climatic driver. Suggestions of collapse in small herbivore cycles since the 1980s have raised concerns about the loss of essential ecosystem functions. Whether such phenomena are general and result from extrinsic environmental changes or from intrinsic process stochasticity is currently unknown. Using a large compilation of time series of vole abundances, we demonstrate consistent cycle amplitude dampening associated with a reduction in winter population growth, although regulatory processes responsible for cyclicity have not been lost. The underlying syndrome of change throughout Europe and grass-eating vole species suggests a common climatic driver. Increasing intervals of low-amplitude small herbivore population fluctuations are expected in the future, and these may have cascading impacts on trophic webs across ecosystems.

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.

Effects of Testosterone on Breeding Density, Breeding Success and Survival of Red Grouse

Territorial intolerance can limit bird numbers by preventing subordinates from holding territories and breeding. We report the first controlled and replicated experiment in a natural population of territorial animals which shows that population density can be decreased by implants of testosterone inducing increased aggressiveness. Implanted territorial cocks expanded their territories at the expense of unimplanted neighbours, some of which left the study area. The probability of an unimplanted cock leaving the study area increased with his number of implanted neighbours. Implanted cocks had better breeding success but poorer subsequent survival than control cocks.

Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects

Resting metabolic rates at thermoneutral (RMRts) are unexpectedly variable. One explanation is that high RMRts intrinsically potentiate a greater total daily energy expenditure (DEE), but recent work has suggested that DEE is extrinsically defined by the environment, which independently affects RMRt. This extrinsic effect could occur because expenditure is forced upwards in poor habitats or enabled to rise in good habitats. We provide here an intraspecific test for an association between RMRt and DEE that separates intrinsic from extrinsic effects and forcing from enabling effects. We measured the DEE and RMRt of 75 free-living short-tailed field voles at two time points in late winter. Across all sites, there was a positive link between individual variation in RMRt and DEE. This correlation, however, emerged only because of an effect across sites, rather than because of an intrinsic association within sites. We defined site quality from the survivorship of voles at the sites and the time at which they commenced breeding in spring. The associations between DEE/RMRt and site quality suggested that in February voles in poorer sites had higher energy demands, indicating that DEE was forced upwards, but in March the opposite was true, with higher demands in good sites, indicating that high expenditure was enabled. These data show that daily energy demands are extrinsically defined, with a link to RMRt that is secondary or independent. Both forcing and enabling effects of the environment may pertain at different times of year.

Host–pathogen time series data in wildlife support a transmission function between density and frequency dependence

A key aim in epidemiology is to understand how pathogens spread within their host populations. Central to this is an elucidation of a pathogens transmission dynamics. Mathematical models have generally assumed that either contact rate between hosts is linearly related to host density (density-dependent) or that contact rate is independent of density (frequency-dependent), but attempts to confirm either these or alternative transmission functions have been rare. Here, we fit infection equations to 6 years of data on cowpox virus infection (a zoonotic pathogen) for 4 natural populations to investigate which of these transmission functions is best supported by the data. We utilize a simple reformulation of the traditional transmission equations that greatly aids the estimation of the relationship between density and host contact rate. Our results provide support for an infection rate that is a saturating function of host density. Moreover, we find strong support for seasonality in both the transmission coefficient and the relationship between host contact rate and host density, probably reflecting seasonal variations in social behavior and/or host susceptibility to infection. We find, too, that the identification of an appropriate loss term is a key component in inferring the transmission mechanism. Our study illustrates how time series data of the host–pathogen dynamics, especially of the number of susceptible individuals, can greatly facilitate the fitting of mechanistic disease models.