Ecological drivers of guanaco recruitment: variable carrying capacity and density dependence

Ungulates living in predator-free reserves offer the opportunity to study the influence of food limitation on population dynamics without the potentially confounding effects of top-down regulation or livestock competition. We assessed the influence of relative forage availability and population density on guanaco recruitment in two predator-free reserves in eastern Patagonia, with contrasting scenarios of population density. We also explored the relative contribution of the observed recruitment to population growth using a deterministic linear model to test the assumption that the studied populations were closed units. The observed densities increased twice as fast as our theoretical populations, indicating that marked immigration has taken place during the recovery phase experienced by both populations, thus we rejected the closed-population assumption. Regarding the factors driving variation in recruitment, in the low- to medium-density setting, we found a positive linear relationship between recruitment and surrogates of annual primary production, whereas no density dependence was detected. In contrast, in the high-density scenario, both annual primary production and population density showed marked effects, indicating a positive relationship between recruitment and per capita food availability above a food-limitation threshold. Our results support the idea that environmental carrying capacity fluctuates in response to climatic variation, and that these fluctuations have relevant consequences for herbivore dynamics, such as amplifying density dependence in drier years. We conclude that including the coupling between environmental variability in resources and density dependence is crucial to model ungulate population dynamics; to overlook temporal changes in carrying capacity may even mask density dependence as well as other important processes.     

Population and prehistory I: Food-dependent population growth in constant environments

We present a demographic model that describes the feedbacks between food supply, human mortality and fertility rates, and labor availability in expanding populations, where arable land area is not limiting. This model provides a quantitative framework to describe how environment, technology, and culture interact to influence the fates of preindustrial agricultural populations. We present equilibrium conditions and derive approximations for the equilibrium population growth rate, food availability, and other food-dependent measures of population well-being. We examine how the approximations respond to environmental changes and to human choices, and find that the impact of environmental quality depends upon whether it manifests through agricultural yield or maximum (food-independent) survival rates. Human choices can complement or offset environmental effects: greater labor investments increase both population growth and well-being, and therefore can counteract lower agricultural yield, while fertility control decreases the growth rate but can increase or decrease well-being. Finally we establish equilibrium stability criteria, and argue that the potential for loss of local stability at low population growth rates could have important consequences for populations that suffer significant environmental or demographic shocks.     

Direct negative density‐dependence in a pond‐breeding frog population

Understanding population dynamics is critical for the management of animal populations. Comparatively little is known about the relative importance of endogenous (i.e. density‐dependent) and exogenous (i.e. density‐independent) factors on the population dynamics of amphibians with complex life cycles. We examined the potential effects of density‐dependent and ‐independent (i.e. climatic) factors on population dynamics by analyzing a 15‐yr time series data of the agile frog Rana dalmatina population from Târnava Mare Valley, Romania. We used two statistical models: 1) the partial rate correlation function to identify the feedback structure and the potential time lags in the time series data and 2) a Gompertz state‐space model to simultaneously investigate direct and delayed density dependence as well as climatic effects on population growth rate. We found evidence for direct negative density dependence, whereas delayed density dependence and climate did not show a strong influence on population growth rate. Here we demonstrated that direct density dependence rather than delayed density dependence or climate determined the dynamics of our study population. Our results confirm the findings of many experimental studies and suggest that density dependence may buffer amphibian populations against environmental stress. Consequently, it may not be easy to scale up from individual‐level effects to population‐level effects.     

Main determinants of rodent population fluctuations in managed Central European temperate lowland forests

Whilst studies have shown that climatic (North Atlantic Oscillation (NAO)) and biotic (acorn production) factors influence rodent populations, mechanisms driving temporal and spatial fluctuation of rodent populations are understudied. This study evaluates relationships between the influence of environmental factors (biotic and abiotic) and phenotypic characteristics across two rodent feeding guilds (granivorous and non-granivorous species) represented by four species of rodents in Central Europe. We hypothesise that the relationship between acorn density and population growth rate are indirectly affected by climatic factors (winter NAO) and that these effects differ amongst herbivorous and granivorous species. In addition, we also tested whether effects of weather and competition on individual phenotype characteristic vary amongst mast and non-mast years. Rodent populations were estimated by catching individuals in snap traps during the growing season (from March to November) over a period of 9 years at three sites. The results of the generalised linear model provide evidence that acorn production best explained the population fluctuations. We therefore conclude that the between-year population fluctuations in rodent abundance were governed by density dependence and initiated primarily by acorn mast years. Auto-regressive models also revealed direct density dependence in combination with the direct effects of mast years. Therefore, strong intraspecific competition for food is likely in years following mast years. Our results also showed that abundance of non-granivorous species is mainly influenced by local weather conditions which could regulate food quality and abundance. On the other hand, population dynamics of granivorous species are caused directly by acorn density and indirectly by climatic condition influencing acorn production.     

Individual‐based modelling of resource competition to predict density‐dependent population dynamics: a case study with white storks

Density regulation influences population dynamics through its effects on demographic rates and consequently constitutes a key mechanism explaining the response of organisms to environmental changes. Yet, it is difficult to establish the exact form of density dependence from empirical data. Here, we developed an individual‐based model to explore how resource limitation and behavioural processes determine the spatial structure of white stork Ciconia ciconia populations and regulate reproductive rates. We found that the form of density dependence differed considerably between landscapes with the same overall resource availability and between home range selection strategies, highlighting the importance of fine‐scale resource distribution in interaction with behaviour. In accordance with theories of density dependence, breeding output generally decreased with density but this effect was highly variable and strongly affected by optimal foraging strategy, resource detection probability and colonial behaviour. Moreover, our results uncovered an overlooked consequence of density dependence by showing that high early nestling mortality in storks, assumed to be the outcome of harsh weather, may actually result from density dependent effects on food provision. Our findings emphasize that accounting for interactive effects of individual behaviour and local environmental factors is crucial for understanding density‐dependent processes within spatially structured populations. Enhanced understanding of the ways animal populations are regulated in general, and how habitat conditions and behaviour may dictate spatial population structure and demographic rates is critically needed for predicting the dynamics of populations, communities and ecosystems under changing environmental conditions.     

Density dependent population growth of the two-spotted spider mite, Tetranychus urticae, on the host plant Leonurus cardiaca

We observed Tetranychus urticae (Koch), a polyphagous spider mite herbivore, on Leonurus cardiaca (L.) at several sites in eastern North America at variable density, ranging from extremely dense to sparse. To understand the nature of T. urticae 's population dynamics we experimentally manipulated population densities on L. cardiaca and assessed per capita growth after 1 to 2 generations in laboratory and field experiments. In particular, we took a 'bottom-up' approach, manipulating both plant size and quality to examine effects on mite dynamics. Per capita growth was strongly dependent on the initial density of the mite population. Spider mite populations grew (1) in a negatively density dependent manner on small plants and (2) unhindered by density dependence on large plants. Mean per capita growth was 59% higher on small plants compared to large plants, irrespective of mite density. We also found evidence for density dependent induced susceptibility to spider mites in small plants and density dependent induced resistance in large plants. Hence, spider mite populations grew at a relatively fast rate on small plants, and this was associated with negative density dependence due to factors that depress population growth, such as food deterioration or limitation. On large plants, spider mite populations grew at a relatively slow rate, apparently resulting in herbivore densities that may not have been high enough to cause intraspecific competition or other forms of negative density dependence.     

Density dependence forces divergent population growth rates and alters occupancy patterns of a central place foraging Antarctic seabird

Density‐dependent regulation is an important process in spatio‐temporal population dynamics because it can alter the effects of synchronizing processes operating over large spatial scales. Most frequently, populations are regulated by density dependence when higher density leads to reduced individual fitness and population growth, but inverse density dependence can also occur when small populations are subject to higher extinction risks. We investigate whether density‐dependent regulation influences population growth for the Antarctic breeding Adélie penguin Pygoscelis adeliae. Understanding the prevalence and nature of density dependence for this species is important because it is considered a sentinel species reflecting the impacts of fisheries and environmental change over large spatial scales in the Southern Ocean, but the presence of density dependence could introduce uncertainty in this role. Using data on population growth and indices of resource availability for seven regional Adélie penguin populations located along the East Antarctic coastline, we find compelling evidence that population growth is constrained at some locations by the amount of breeding habitat available to individuals. Locations with low breeding habitat availability had reduced population growth rates, higher overall occupancy rates, and higher occupancy of steeper slopes that are sparsely occupied or avoided at other locations. Our results are consistent with evolutionary models of avian breeding habitat selection where individuals search for high‐quality nest sites to maximize fitness returns and subsequently occupy poorer habitat as population density increases. Alternate explanations invoking competition for food were not supported by the available evidence, but strong conclusions on food‐related density dependence were constrained by the paucity of food availability data over the large spatial scales of this region. Our study highlights the importance of incorporating nonconstant conditions of species–environment relationships into predictive models of species distributions and population dynamics, and provides guidance for improved monitoring of fisheries and climate change impacts in the Southern Ocean.     

Interaction between seasonal density-dependence structures and length of the seasons explain the geographical structure of the dynamics of voles in Hokkaido: an example of seasonal forcing

The grey-sided vole (Clethrionomys rufocanus) is distributed over the entire island of Hokkaido, Japan, across which it exhibits multi-annual density cycles in only parts of the island (the north-eastern part); in the remaining part of the island, only seasonal density changes occur. Using annual sampling of 189 grey-sided vole populations, we deduced the geographical structure in their second-order density dependence. Building upon our earlier suggestion, we deduce the seasonal density-dependent structure for these populations. Strong direct and delayed density dependence is found to occur during winter, whereas no density dependence is seen during the summer period. The direct density dependence during winter may be seen as a result of food being limited during that season: the delayed density dependence during the winter is consistent with vole-specialized predators (e.g. the least weasel) responding to vole densities so as to have a negative effect on the net growth rate of voles in the following year. We conclude that the observed geographical structure of the population dynamics may be properly seen as a result of the length of the summer in interaction with the differential seasonal density-dependent structure. Altogether, this indicates that the geographical pattern in multi-annual density dynamics in the grey-sided vole may be a result of seasonal forcing.     

Complex consequences of increased density for reproductive output in an invasive freshwater snail

Population density can have profound, often negative effects on fitness-related traits and population dynamics, and density dependence is of central importance to many prominent ecological and evolutionary hypotheses. Here, we used experimental manipulations of food, population density, and water conditioning to characterize the mechanisms underlying reproductive density-dependence in Potamopyrgus antipodarum. This New Zealand freshwater snail is a prominent model system for invasion biology, ecotoxicology, and the maintenance of sexual reproduction. We demonstrated that a primary source of negative density-dependence is food limitation, but surprisingly, we found that P. antipodarum reproductive output was much higher in high density versus low-density conditions when food was adequate. We then used manipulations of water environment to demonstrate that these positive effects of high density are likely caused by a waterborne substance produced by P. antipodarum. Altogether, these results indicate that there are strong and complex connections between food availability, density, and reproductive output in this important model system that could influence the dynamics of invasive populations, the costs and benefits of sex, and the approaches used for ecotoxicology studies.     

Intrinsic and extrinsic determinants of mountain pine beetle population growth

1 Mountain pine beetle Dendroctonus ponderosae populations have large, economically significant outbreaks. Density dependence and environmental variability are expected to have important effects on their dynamics. We analysed time series data from an outbreak in the 1930s to determine the relative importance of population density and environmental variability on local population growth rates.
2 Resource depletion occurred rapidly at the scale of 0.4 ha and population growth rates were strongly density dependent. Annual environmental changes did not have detectable effects on population growth rates, leading to the conclusion that intrinsic processes influenced local population density more than extrinsic factors during this outbreak.
3 Our calculated value of r _max (1.16) does not suggest intrinsically cyclic population dynamics. Our estimate of r _max and density dependence will be useful in developing applied models of mountain pine beetle outbreaks, and the subsequent evaluation of management strategies.     

Density-dependent processes in the life history of fishes: evidence from laboratory populations of zebrafish Danio rerio

Population regulation is fundamental to the long-term persistence of populations and their responses to harvesting, habitat modification, and exposure to toxic chemicals. In fish and other organisms with complex life histories, regulation may involve density dependence in different life-stages and vital rates. We studied density dependence in body growth and mortality through the life-cycle of laboratory populations of zebrafish Danio rerio. When feed input was held constant at population-level (leading to resource limitation), body growth was strongly density-dependent in the late juvenile and adult phases of the life-cycle. Density dependence in mortality was strong during the early juvenile phase but declined thereafter and virtually ceased prior to maturation. Provision of feed in proportion to individual requirements (easing resource limitation) removed density dependence in growth and substantially reduced density dependence in mortality, thus indicating that 'bottom-up' effects act on growth as well as mortality, but most strongly on growth. Both growth and mortality played an important role in population regulation, with density-dependent growth having the greater impact on population biomass while mortality had the greatest impact on numbers. We demonstrate a clear ontogenic pattern of change in density-dependent processes within populations of a very small (maximum length 5 mm) fish, maintained in constant homogeneous laboratory conditions. The patterns are consistent with those distilled from studies on wild fish populations, indicating the presence of broad ontogenic patterns in density-dependent processes that are invariant to maximum body size and hold in homogeneous laboratory, as well as complex natural environments.     

Population growth rate and its determinants: an overview

We argue that population growth rate is the key unifying variable linking the various facets of population ecology. The importance of population growth rate lies partly in its central role in forecasting future population trends; indeed if the form of density dependence were constant and known, then the future population dynamics could to some degree be predicted. We argue that population growth rate is also central to our understanding of environmental stress: environmental stressors should be defined as factors which when first applied to a population reduce population growth rate. The joint action of such stressors determines an organism's ecological niche, which should be defined as the set of environmental conditions where population growth rate is greater than zero (where population growth rate = r = log(e)(N(t+1)/N(t))). While environmental stressors have negative effects on population growth rate, the same is true of population density, the case of negative linear effects corresponding to the well-known logistic equation. Following Sinclair, we recognize population regulation as occurring when population growth rate is negatively density dependent. Surprisingly, given its fundamental importance in population ecology, only 25 studies were discovered in the literature in which population growth rate has been plotted against population density. In 12 of these the effects of density were linear; in all but two of the remainder the relationship was concave viewed from above. Alternative approaches to establishing the determinants of population growth rate are reviewed, paying special attention to the demographic and mechanistic approaches. The effects of population density on population growth rate may act through their effects on food availability and associated effects on somatic growth, fecundity and survival, according to a 'numerical response', the evidence for which is briefly reviewed. Alternatively, there may be effects on population growth rate of population density in addition to those that arise through the partitioning of food between competitors; this is 'interference competition'. The distinction is illustrated using a replicated laboratory experiment on a marine copepod, Tisbe battagliae. Application of these approaches in conservation biology, ecotoxicology and human demography is briefly considered. We conclude that population regulation, density dependence, resource and interference competition, the effects of environmental stress and the form of the ecological niche, are all best defined and analysed in terms of population growth rate.     

Comparative population dynamics of large and small mammals in the Northern Hemisphere: deterministic and stochastic forces

Deterministic feedbacks within populations interact with extrinsic, stochastic processes to generate complex patterns of animal abundance over time and space. Animals inherently differ in their responses to fluctuating environments due to differences in body sizes and life history traits. However, controversy remains about the relative importance of deterministic and stochastic forces in shaping population dynamics of large and small mammals. We hypothesized that effects of environmental stochasticity and density dependence are stronger in small mammal populations relative to their effects in large mammal populations and thus differentiate the patterns of population dynamics between them. We conducted an extensive, comparative analysis of population dynamics in large and small mammals to test our hypothesis, using seven population parameters to describe general dynamic patterns for 23 (14 species) time series of observations of abundance of large mammals and 38 (21 species) time series for small mammals. We used state‐space models to estimate the strength of direct and delayed density dependence as well as the strength of environmental stochasticity. We further used phylogenetic comparative analysis to detect differences in population dynamic patterns and individual population parameters, respectively, between large and small mammals. General population dynamic patterns differed between large and small mammals. However, the strength of direct and delayed density dependence was comparable between large and small mammals. Moreover, the variances of population growth rates and environmental stochasticity were greater in small mammals than in large mammals. Therefore, differences in population response to stochastic forces and strength of environmental stochasticity are the primary factor that differentiates population dynamic patterns between large and small mammal species.     

The Role of Density Regulation in Extinction Processes and Population Viability Analysis

We review the role of density dependence in the stochastic extinction of populations and the role density dependence has played in population viability analysis (PVA) case studies. In total, 32 approaches have been used to model density regulation in theoretical or applied extinction models, 29 of them are mathematical functions of density dependence, and one approach uses empirical relationships between density and survival, reproduction, or growth rates. In addition, quasi-extinction levels are sometimes applied as a substitute for density dependence at low population size. Density dependence further has been modelled via explicit individual spacing behaviour and/or dispersal. We briefly summarise the features of density dependence available in standard PVA software, provide summary statistics about the use of density dependence in PVA case studies, and discuss the effects of density dependence on extinction probability. The introduction of an upper limit for population size has the effect that the probability of ultimate extinction becomes 1. Mean time to extinction increases with carrying capacity if populations start at high density, but carrying capacity often does not have any effect if populations start at low numbers. In contrast, the Allee effect is usually strong when populations start at low densities but has only a limited influence on persistence when populations start at high numbers. Contrary to previous opinions, other forms of density dependence may lead to increased or decreased persistence, depending on the type and strength of density dependence, the degree of environmental variability, and the growth rate. Furthermore, effects may be reversed for different quasi-extinction levels, making the use of arbitrary quasi-extinction levels problematic. Few systematic comparisons of the effects on persistence between different models of density dependence are available. These effects can be strikingly different among models. Our understanding of the effects of density dependence on extinction of metapopulations is rudimentary, but even opposite effects of density dependence can occur when metapopulations and single populations are contrasted. We argue that spatially explicit models hold particular promise for analysing the effects of density dependence on population viability provided a good knowledge of the biology of the species under consideration exists. Since the results of PVAs may critically depend on the way density dependence is modelled, combined efforts to advance statistical methods, field sampling, and modelling are urgently needed to elucidate the relationships between density, vital rates, and extinction probability.     

Late Glacial and Early Holocene human demographic responses to climatic and environmental change in Atlantic Iberia

Successive generations of hunter–gatherers of the Late Glacial and Early Holocene in Iberia had to contend with rapidly changing environments and climatic conditions. This constrained their economic resources and capacity for demographic growth. The Atlantic façade of Iberia was occupied throughout these times and witnessed very significant environmental transformations. Archaeology offers a perspective on how past human population ecologies changed in response to this scenario. Archaeological radiocarbon data are used here to reconstruct demographics of the region over the long term. We introduce various quantitative methods that allow us to develop palaeodemographic and spatio-temporal models of population growth and density, and compare our results to independent records of palaeoenvironmental and palaeodietary change, and growth rates derived from skeletal data. Our results demonstrate that late glacial population growth was stifled by the Younger Dryas stadial, but populations grew in size and density during the Early to Middle Holocene transition. This growth was fuelled in part by an increased dependence on marine and estuarine food sources, demonstrating how the environment was linked to demographic change via the resource base, and ultimately the carrying capacity of the environment.This article is part of the theme issue ‘Cross-disciplinary approaches to prehistoric demography’.     

Density dependence and microevolution interactively determine effects of phenology mismatch on population dynamics

Life cycle events in plants and animals are typically adaptively tuned to anticipate predictable seasonal changes in environmental conditions or resources. Climate change is expected to affect the temporal component of species’ interactions, e.g. by creating a mismatch between a predator's breeding time (when ample food supply is critical) and the time when prey abundance is high. The demographic implications of such a mismatch remain unclear, however. Here we focussed on changes in the phenology of consumers relative to that of their food. We developed a model where reproductive output of the consumer up to offspring independence depended on mismatch and recruitment of the offspring to breeders depended on offspring density according to a Beverton–Holt function. Using a deterministic version of the model, we clarified how the effects of (constant) mismatch on equilibrium population size depended on the emergent strength of negative density dependence (DD). Using a stochastic, individual‐based version, we showed that when the environment changed abruptly, the rate of population recovery was faster when heritability of seasonal timing was higher and DD was stronger. When the environment shifted continuously, the rate of decline in population size was inversely proportional to the rate of microevolution, but stronger DD slowed the rate of decline for a given heritability and thus effectively ‘bought time’ for evolutionary rescue. These results highlight the importance of negative DD, which interacts with the effects of trait heritability and stabilizing selection strength, in influencing the fate of populations experiencing environmental change. We emphasize, however, that outcomes in nature will depend crucially on the exact nature of DD, in particular whether population growth rate differences are greatest at low or high densities, highlighting the need for empirical comparisons of compensatory processes in different populations or species.     

Density-dependent regulation of natural and laboratory rotifer populations

Density-dependent regulation of abundance is fundamentally important in the dynamics of most animal populations. Density effects, however, have rarely been quantified in natural populations, so population models typically have a large uncertainty in their predictions. We used models generated from time series analysis to explore the form and strength of density-dependence in several natural rotifer populations. Population growth rate (r) decreased linearly or non-linearly with increased population density, depending on the rotifer species. Density effects in natural populations reduced r to 0 at densities of 1–10 l^–1 for 8 of the 9 rotifer species investigated. The sensitivities of these species to density effects appeared normally distributed, with a mean r=0 density of 2.3 l^–1 and a standard deviation of 1.9. Brachionus rotundiformis was the outlier with 10–100× higher density tolerance. Density effects in laboratory rotifer populations reduced r to 0 at population densities of 10–100 ml^–1, which is 10⁴ higher than densities in natural populations. Density effects in laboratory populations are due to food limitation, autotoxicity or to their combined effects. Experiments with B. rotundiformis demonstrated the absence of autotoxicity at densities as high as 865 ml^–1, a much higher density than observed in natural populations. It is, therefore, likely that food limitation rather than autotoxicity plays a major role in regulating natural rotifer populations.     

Patterns and dynamics of rapid local adaptation and sex in varying habitat types in rotifers

Local adaptation is an important principle in a world of environmental change and might be critical for species persistence. We tested the hypothesis that replicated populations can attain rapid local adaptation under two varying laboratory environments. Clonal subpopulations of the cyclically parthenogenetic rotifer Brachionus calyciflorus were allowed to adapt to two varying harsh and a benign environment: a high‐salt, a food‐limited environment and untreated culture medium (no salt addition, high food). In contrast to most previous studies, we re‐adjusted rotifer density to a fixed value (two individuals per ml) every 3–4 days of unrestricted population growth, instead of exchanging a fixed proportion of the culture medium. Thus our dilution regime specifically selected for high population growth during the entire experiment and it allowed us to continuously track changes in fitness (i.e., maximum population growth under the prevailing conditions) in each population. After 56 days (43 asexual and eight sexual generations) of selection, the populations in the harsh environments showed a significant increase in fitness over time relative to the beginning compared to the population in untreated culture medium. Furthermore, the high‐salt population exhibited a significantly elevated ratio of sexual offspring from the start of the experiment, which suggested that this environment either triggered higher rates of sex or that the untreated medium and the food‐limited environment suppressed sex. In a following assay of local adaptation we measured population fitness under “local” versus “foreign” conditions (populations adapted to this environment compared to those of the other environment) for both harsh habitats. We found significantly higher fitness values for the local populations (on average, a 38% higher fitness) compared to the foreign populations. Overall, local adaptation was formed rapidly and it seemed to be more pronounced in the high‐salt treatment.     

Direct and socially-mediated effects of food availability late in life on life-history variation in a short-lived lizard

Food availability is a major environmental factor that can influence life history within and across generations through direct effects on individual quality and indirect effects on the intensity of intra- and intercohort competition. Here, we investigated in yearling and adult common lizards (Zootoca vivipara) the immediate and delayed life-history effects of a prolonged food deprivation in the laboratory. We generated groups of fully fed or food-deprived yearlings and adults at the end of one breeding season. These lizards were released in 16 outdoor enclosures together with yearlings and adults from the same food treatment and with food-deprived or fully fed juveniles, creating four types of experimental populations. Experimental populations were then monitored during 2 years, which revealed complex effects of food on life-history trajectories. Food availability had immediate direct effects on morphology and delayed direct effects on immunocompetence and female body condition at winter emergence. Also, male annual survival rate and female growth rate and body size were affected by an interaction between direct effects of food availability and indirect effects on asymmetric competition with juveniles. Reproductive outputs were insensitive to past food availability, suggesting that female common lizards do not solely rely on stored energy to fuel reproduction. Finally, food conditions had socially-mediated intergenerational effects on early growth and survival of offspring through their effects on the intensity of competition. This study highlights the importance of social interactions among cohorts for life-history trajectories and population dynamics in stage-structured populations.     

Mechanisms of density dependence in fluctuating vole populations: deducing annual density dependence from seasonal processes

Based on recent advances in time-series analyses of ecological dynamics using statistical and mathematical models, we summarise our recent results on the seasonal processes in the annual population dynamics of the grey-sided vole Clethrionomys rufocanus (Sundevall, 1846) in Hokkaido, Japan, and report additional analyses on annual and seasonal density dependence. Annual direct density dependence was strong in almost all populations. In contrast, delayed density dependence was generally weak, although clear delayed density dependence was detected in some of the studied populations. Although seasonal density dependence was observed both in winter and summer, direct density dependence was much more profound during winter; thus, winter density dependence contributed most to the overall annual direct density dependence. We found no correlation between the seasonal components of annual direct density dependence; however, the corresponding seasonal components for annual delayed density dependence were positively correlated. We conclude that winter conditions influence the strength of annual direct density dependence most profoundly. Moreover, we conclude that direct density dependence during summer and winter may be generated by different mechanisms, whereas delayed density dependence seems to be generated by a common mechanism. Candidate mechanisms are discussed in relation to general knowledge of northern rodent populations and to specific insights provided by earlier studies of grey-sided voles in Hokkaido.