Journal of Ecology 2009, 97, 666 674

Blackwell Publishing Ltd

doi: 10.1111/j.1365-2745.2009.01504.x

Linking environmental variation to population dynamics of a forest herb

Johan P Dahlgren* and Johan Ehrln .

Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden

Summary 1. Although necessary for understanding and predicting population dynamics, abiotic and biotic interactions have only rarely been coupled to demography and population dynamics. 2. We estimated effects of 11 environmental factors on survival, growth and fertility of the perennial herb Actaea spicata and incorporated signicant factors into integral projection models to assess their effect on population dynamics. 3. Statistical models suggested that high soil potassium concentration increased individual growth and that seed predation and, to a lesser extent, canopy cover reduced seed production. 4. Demographic models showed that both soil potassium concentration and pre-dispersal seed predation could reverse population growth from positive to negative. The observed range of soil potassium concentration corresponded to growth rates () between 0.96 and 1.07, at mean observed seed predation intensity. At observed mean potassium concentration, growth rate ranged from 0.99 to 1.02 over observed seed predation intensities. 5. Sensitivity of population growth rate to different vital rates strongly inuenced the relative effects of the two factors. Elasticity analysis suggested that proportional changes in soil potassium concentration result in seven times larger effects on population growth rate than changes in seed predation. 6. Synthesis. We conclude that relatively weak associations between environmental factors and vital rates can have substantial long-term effects on population growth. Approaches based on detailed demographic models, that simultaneously assess abiotic and biotic effects on population growth rate, constitute important tools for establishing the links between the environment and dynamics of populations and communities. Key-words: Actaea spicata, habitat range, integral projection model, plant demography, population dynamics, pre-dispersal seed predation, soil potassium concentration

Introduction
The relationship between abiotic and biotic interactions and the dynamics of populations constitutes a fundamental question in ecology (cf. Gleason 1926). The ultimate effects of environmental factors on population dynamics are evident from correlations between differences in environment and species distributions, densities and population sizes (e.g. Guisan & Zimmermann 2000; Pearce & Boyce 2006). However, the mechanisms behind these relationships have been relatively little studied. Any factor inuencing population dynamics must be acting via affecting survival, fertility or individual growth rates, which together determine population growth
*Correspondence author. E-mail: johan.dahlgren@botan.su.se

rate (Caswell 2001). Patterns of species abundances and distributions are, in turn, largely the cumulative result of differences in population growth rates between environments. Population growth rates are, however, determined not only by the surrounding environment but also by intraspecic densities (Halpern & Underwood 2006). Linking environmental effects and population densities to differences in vital rates thus constitutes a way to unravel the mechanisms governing species abundances and distributions. From a conservation perspective it is necessary to understand how the environment affects vital rates in order to increase accuracy of population viability analyses (e.g. Morris & Doak 2002) and design appropriate management actions (e.g. Ehrln et al. 2005). Furthermore, knowledge of the links between vital rates and environmental factors combined with information on how

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Linking environment and population dynamics 667 these factors change over time can be used to predict population growth and viability in changing environments (cf. Gotelli & Ellison 2006). This is particularly important as many natural populations are inuenced by climate change, eutrophication and succession, and many populations of rare and threatened species occur in environments that undergo change (Caughley 1994; Norris 2004). The assumption that abiotic and biotic environmental factors dene niche boundaries of species is central to ecology (Kingsland 1991). Still, effects of abiotic or biotic factors on plant population dynamics have only rarely been examined and, to our knowledge, never simultaneously. Results from demographic studies on populations in different environments suggest that abiotic environmental factors, such as light availability (Alvarez-Buylla 1994), nutrient concentrations (Gotelli & Ellison 2002; Brys et al. 2005; Colling & Matthies 2006), ooding (Smith et al. 2005) and history of catastrophic events (Menges & Kimmich 1996; Pascarella & Horvitz 1998), can have substantial effects on plant population growth rates. Biotic interactions such as negative relationships between the intensity of herbivory and plant population growth rates found in some systems can also restrict species distributions and abundances (Horvitz et al. 2005; Rose et al. 2005; Maron & Crone 2006; Kolb et al. 2007). In addition, competition may be the cause of variability in population growth rates between patches with different co-occurring species (Williams & Crone 2006). Taken together these studies suggest that population dynamics are determined by multiple interactions with the environment. Advances in computer technology and new modelling tools now enable researchers to assess such simultaneous effects of multiple environmental factors by explicitly including them in structured demographic models (Easterling et al. 2000; Ellner & Rees 2006). Here we investigate how abiotic and biotic environmental factors inuence the demography of Actaea spicata L., a longlived perennial forest herb. In the study area, A. spicata occurs in shaded nutrient-rich patches (Mossberg & Stenberg 2003) and individuals often suffer losses of more than 50% of their total seed number to a specialized insect predator (von Zeipel et al. 2006). For the present study, detailed demographic and environmental data were collected over 3 years from a total of 1323 individuals. We estimated levels of eight abiotic environmental factors and seed predation for each individual. We also included measures of intra- and interspecic density to test for density dependence. Analyses were carried out in two steps. First, we used multiple regression modelling to determine how properties of the local environment inuence plant survival, growth and fecundity. Secondly, we incorporated those two aspects of the environment that were identied as the most important in the statistical analyses into size-structured integral projection models (IPMs), and estimated population growth rates for different combinations of these two environmental variables. We use the results to assess effects of the examined biotic and abiotic interactions on population growth and suggest that this approach is useful for achieving a mechanistic understanding of how environmental factors inuence population dynamics and species distributions.

Methods
STUDY SPECIES AND AREA

Baneberry (Actaea spicata L. Ranunculaceae) is distributed over most of Europe and parts of Asia (Germplasm Resources Information Network, www.ars-grin.gov/). In northern Europe it occurs in shady, well-drained habitats in nutrient-rich deciduous forests and mixed deciduous and coniferous forests, often on limestone (Pellmyr 1984). The estimated mean life span of individuals surviving to reproduction is 20.2 years (J. Ehrln & J.P. Dahlgren, unpublished data). The growth form is typical of an early summer owering forest herb, that is, it has a greater height than spring ephemerals and an umbrella-like leaf display (cf. Givnish 1987). Individuals usually produce one or two, but sometimes up to ve shoots in the study area. Single shoots produce up to four inorescences (Eriksson 1995), each consisting of 130 white owers. Primary inorescences typically contain the majority of owers. The fruit is a black berry, usually containing 816 seeds (von Zeipel 2007). Seeds germinate producing a radicle, normally 1 year after release, while cotyledons emerge 1 year after germination (Ehrln & Eriksson 2000; Frborg & Eriksson 2003). Vegetative propagation has never been recorded and new individuals originate from seeds (J.P. Dahlgren, unpublished data). Earlier emergence of shoots in spring and earlier owering are correlated with higher nutrient concentrations, in particular of potassium and phosphorus (Dahlgren et al. 2007). High soil potassium concentration has been shown to result in increased growth of individuals (Salomonson et al. 1992). In the study area, pre-dispersal seed predation by a specialist moth, Eupithecia immundata (Geometridae), apparently constitutes the most important biotic interaction for A. spicata. Oviposition by the seed predator occurs in a short period from mid-June to early July, almost exclusively affecting primary infructescences (Eriksson 1995). Typically, one larva is developed per fruit. After consuming most of the seeds, the larva eats its way out in mid-July to August, leaving an exit hole. Average predation rates within patches in the study area range from 0% to 100% of fruits in primary infructescences (von Zeipel et al. 2006). The entire plant is toxic and the only other known herbivores are the specialized Eupithecia actaeata feeding on the leaves late in the season, generalist rodents feeding on dispersed seeds and molluscs feeding on seedlings (J. Ehrln & J.P. Dahlgren, personal observation; Frborg 2001). Potential pollinators include several insect orders, but most reported visitors belong to Coleoptera and Diptera (Pellmyr 1984). Fruit set is close to 100%, suggesting that variation in pollination is unlikely to have important effects on seed production (Pellmyr 1984; Eriksson 1995). The study was conducted on four patches of A. spicata in the forests of Tullgarn natural reserve, 45 km SSW of Stockholm, Sweden (586 N, 174 E), hereafter referred to as sites. Distances between sites varied from 0.8 to 2 km. The tree ora ranged from pure deciduous stands, consisting mainly of pedunculate oak (Quercus robur) and hazel (Corylus avellana) to coniferous stands dominated by Norway spruce (Picea abies). Actaea spicata was abundant at all sites.

DATA COLLECTION

In 2004, ve to seven 5 5 m plots were established and 200 non-seedling individuals were marked at each site (25 plots in total). Censuses were made in 2004, 2005, 2006 and 2007. Presence (0 or 1), shoot diameters, plant height and total fruit number were recorded for all non-seedling individuals each year in JuneJuly. An individual

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Table 1. The 11 environmental factors tested for effects on vital rates and population growth rate of Actaea spicata Environmental factor Ground slope Soil depth May canopy openness July canopy openness Soil potassium* Soil phosphorus* Soil water content* Soil temperature* Interspecic density Intraspecic density Seed predation Mean (unit) SD across individuals 8.50 19.4 13.5 6.62 (cm) 0.62 0.14 0.26 0.10 37.3 13.2 (mg 1001 g) 3.28 1.20 (mg 1001 g) 0.52 0.07 9.55 0.76 (C) 414 807 (cm) 4290 4260 (mm3) 0.20 Description Inclination degree, weighted 1.0 for south-, 0.5 for east- and west-, 1.0 for north-facing slopes Mean of three measurements with a metal stick Proportion of canopy photographs not covered by foliage Proportion of canopy photographs not covered by foliage AL extraction method (Salomon 1998). Samples collected at start of vegetative development AL extraction method (Salomon 1998). Samples collected at start of vegetative development Ratio of the difference between wet and dry mass to dry mass at the time of owering Mean temperature during 6 weeks after shoot emergence, estimated using data loggers Height proportion of ground coverage of vegetation within 30 cm, estimated visually Summed above-ground volume of conspecics within 1 m Mean proportion of fruits attacked over 2004 and 2005 (see text)

*Presented statistics are for interpolated values based on four samples per plot (see text). The mean seed predation rate in the study area (mean SD) was 0.24 0.12 (average means and standard deviations for 150 populations over 4 years; von Zeipel 2007).

was considered dead if it was missing in two consecutive censuses. Individuals that were missing in one census had either been dormant or had their shoots damaged early in the season and wilted before the demographic recording. All seedlings were counted as they emerged and up to 50 were marked per site and year. In total, 335 new individuals were included after 2004. Plant height was dened as the distance from the ground to the horizontal plane formed by the largest leaves. Plant size was estimated by the natural logarithm of the product of plant height and the sum of squared shoot diameters. Alternative examined size measures were less correlated with survival and fertility (not presented). We dened growth of an individual as the difference in size between-years. Yearly individual seed production was calculated as the product of the yearly count of total fruit number and mean number of seeds per fruit in 2005. Mean number of seeds per fruit in 2005 was determined by collecting half of the fruits from primary infructescences, in August when still attached, and counting the number of seeds in intact and preyed fruits (von Zeipel 2007). To maximize spatial resolution of environmental effects on individual vital rates, estimates of environmental variables were calculated for each individual (Table 1). Canopy cover before and after tree leang, ground slope, inter- and intraspecic plant density and seed predation were measured for each individual. Soil concentrations of phosphorus and potassium, soil temperature, soil depth and soil water content were measured in each plot quadrant. The two nutrients were chosen since previous studies have shown that potassium and phosphorus affect the performance of A. spicata individuals (Salomonson et al. 1992; Dahlgren et al. 2007). To use the most likely estimate of the soil variables in the population models, each A. spicata individual was assigned an interpolated value as a mean of the four values available per plot (weighted based on distances between the focal individuals and each of the four sampling points). Because continuous gradients of forest soil characteristics cannot be assumed, our estimated values are only approximations (cf. Lechowicz & Bell 1991). Ideally, measurements should be taken at the actual location of roots of each individual, but

this is hardly possible without harming plants. In addition, effects of smaller-scale spatial heterogeneity are likely reduced by the fact that ne root systems may cover a substantial underground area below each individual (cf. Casper et al . 2003). To the extent that the interpolated values underestimate variation among individuals, this should result in conservative approximations of the effects of soil characteristics on individual plants. Although interpolated values may provide the best possible estimates for each individual and are useful for model parameterization, they are not independent. We therefore tested hypotheses about effects of environmental factors at the plot quadrant level. For a detailed description of the measurements of environmental variables see Dahlgren et al. (2007). In 2004, pre-dispersal fruit predation was recorded in August as the proportion of all fruits with exit holes of larvae. In 2005, fruit predation was calculated as the proportion of fruits in primary infructescences that were preyed, multiplied by the proportion of total fruits that occurred in primary infructescences.

STATISTICAL ANALYSES

The effect of pre-dispersal seed predation on number of seeds per fruit was estimated by comparing mean seed numbers in intact and attacked fruits in 2005. The effects of the remaining ten environmental factors on the individual vital rates (probability of survival, growth, probability of owering, number of fruits and number of seeds per fruit) were examined by including size and the environmental variables in linear and generalized linear models in R 2.7.2 (R development core team, 2007). Only data describing transitions between-years 2004 2005 and 20052006, were used since these regressions were to be used as components of the demographic models and absence in 2007 could not be distinguished from seasonal disappearance or dormancy until 2008. To avoid overestimation of individual growth and fecundity due to the exclusion of dormant plants from analyses, we assigned the size in the year of reappearance also to the year in which individuals were dormant while fecundity was set to zero. Dormant individuals were thus included in the subsequent population

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models although we did not use a separate category for dormant individuals. Growth, fruit number and number of seeds per fruit were modelled as linear regressions (Poisson regression analyses of fruit and seed number yielded similar results) and probabilities of survival and owering were modelled as logistic regressions (by specifying binomial error distributions and logit link functions in generalized linear models). Full multiple regression models of effects on vital rates containing all variables were reduced by removing clearly not signicant variables (P > 0.6) in order to avoid effects of potential overtting (Harrell 2001). Soil potassium and phosphorus were strongly collinear (r > 0.8), and the one out of these two with the weakest effect was removed from the models. Further reduction of models, for example, using stepwise selection based on AIC, was not used in order to avoid models with t and parameter estimates tending to be high (Harrell 2001). Signicance testing of each variable was done in mixed-effects models including also individual, plot quadrant and plot as nested random effects. Variables that were based on interpolations of measures in plot quadrants were included as quadrant-level variables in these tests. For the simple case with potassium as the only (plot quadrant-level) environmental factor and plot quadrant as the only level on which the intercept varies, the model describing individual growth is: yij = 1 + 2zi + 3xij + bi l + ij, eqn 1 n is a distribution function describing the adult population, S2 is the number of seedlings and S1 is the number of seeds. x is size year t and y is size year t + 1. L and U are minimum and maximum possible sizes, respectively. In equation 2, ps is the probability of seedling survival, pd (y) is the probability density function of sizes of surviving seedlings, modelled as a normal distribution with mean and standard deviation from the data, s (x) is the survival function, modelled by logistic regression and g (y, x) is the probability density function of growth. The growth function is modelled as a normal distribution with a mean given by the linear regression of y on x and a standard deviation given by the variance around the regression line. Size limits were set to 1.1 maximum observed size in 2004 (= 15.28) and 0.9 minimum observed size in 2004 (= 0.92). Note that while g (y, x) has to integrate to one, modelling growth as an unbounded normal distribution leads to individuals sometimes becoming smaller or larger than the specied minimum and maximum size classes. This had a minor effect on population growth rate in our model. We adjusted the resulting probabilities in the computer implementation of the model so that the probability of attaining a size outside the range was included in the probability of attaining the respective extreme size. In equation 3, pe is the probability of seedling establishment (and seed survival), calculated as the number of seedlings year t + 2 divided by seed number year t. Thus, seed survival was incorporated in this measure and all seed mortality was considered to take place in year t. In equation 4, pf (x) is the probability of owering, modelled by logistic regression, fn (x) is number of fruits produced, modelled by linear regression and fs is the number of seeds per fruit, calculated as: fs = mpred ppred + mint(1 ppred), eqn 5

where size year t + 1 of individual j in plot quadrant i, yij, is decided by size year t, xij, and potassium in plot quadrant i, zi. s are xed effects, bi1 is the random effect of plot quadrant and ij is the individual error term (cf. Fox 2002). The random effects of individual and plot, accounting for repeated measures of individuals and the spatial structure of the data, respectively, were included when performing signicance tests to avoid pseudoreplication. The lmer (for linear models) and glmer (for generalized linear models) functions in the lme4 package were used to t mixed effects models (Pinheiro & Bates 2000).

INTEGRAL PROJECTION MODELS

IPMs of population dynamics resemble matrix projection models, but instead of a projection matrix, a continuous projection kernel is used and the population size distribution is described by a density function instead of a vector (Easterling et al. 2000). Growth, survival and fertility components are included in the models as functions of one or several state variables, using all sampled individuals for parameterizing each vital rate for a given state (Ellner & Rees 2006). As in most demographic models of long-lived plants, our default state variable was size (Caswell 2001). Environmental factors were included as covariates in the regression models of the vital rate functions. Environmental covariates that were not included explicitly in the IPM were centred in order to set them to their mean values. The model consisted of three coupled equations, allowing a delay of seedling establishment (see Study species and area) and treatment of seeds and seedlings as discrete classes (cf. Rees et al. 2006):
U

n( y, t + 1) = ps pd ( y )S2 (t ) + s( x )g ( y, x )n( x, t )dx;

L

eqn 2 eqn 3

where ppred is the proportion of attacked fruits, mpred is the mean number of intact seeds in attacked fruits and mint is the mean seed number in intact fruits. The IPM was rst used to calculate population growth rate () at the observed mean levels of environmental factors. We also calculated elasticity values for all possible size transitions, based on the stable size and reproductive value distributions of the model (Easterling et al. 2000). Condence intervals of were calculated by bootstrapping, using the R package boot to perform an ordinary nonparametric bootstrap. The same number of individuals as recorded in permanent plots (1270 adults) was resampled with replacement from the data matrix, and all regression coefcients for relationships between vital rates and environmental factors and size were recalculated and used to obtain for each of 10 000 bootstrap replicates. We also calculated for the observed range of the two environmental factors that were identied as most important in the analyses. For each factor we used 20 values, distributed evenly over the observed ranges and we combined values for the two environmental factors in a full-factorial manner. Soil potassium concentration varied from the lowest (9.0 mg per 100 g soil) to the highest (72.6 mg per 100 g soil) observed potassium concentration. The predation level varied from 0 to 0.57 of fruits, which corresponds to the range of mean predation intensities found in A. spicata patches in the area (von Zeipel et al. 2006). Elasticity to a particular environmental factor was calculated as the proportional effect on of a 10% increase from the observed value. The models were run in R 2.7.2 and the code was based on the one provided in Ellner & Rees (2006).

S2(t + 1) = peS1(t);
U

Results
eqn 4

S1(t + 1) = p f ( x ) fn ( x ) fs n( x, t ) dx.
L

Individual plant size had a large inuence on survival, growth, probability of owering and number of fruits, and its

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Table 2. Signicant predictor variables in regression models of survival, growth and fertility of Actaea spicata and log-likelihoods (LL) of models including different combinations of predictor variables. Signicance was tested in models accounting for repeated measures of individuals and the spatial structure of the data (see text for details) LL of model with size and signicant environmental variables NA 1991 (R 2 = 0.563) NA 559.3 (R 2 = 0.253) NA LL of model with size and all environmental variables 436.7 1978 (R 2 = 0.572) 669.0 549.0 (R 2 = 0.278) NA

Response variable Survival Size next year Probability of owering Fruit number Seed number per fruit

Signicant predictor variables Size Size + soil potassium* Size Size + May canopy openness Seed predation

LL of model with only size 451.9 2001 (R 2 = 0.557) 678.0 564.2 (R 2 = 0.240) NA

NA, not applicable. *Soil potassium: b = 0.015, t = 3.87, P = 0.0001. May canopy openness: b = 0.005, t = 2.15, P = 0.03. The effect of seed predation was not tested statistically. There were no signicant effects of environmental factors on seed number per fruit when accounting for seed predation.

Table 3. Components and parameter values of the integral projection models for Actaea spicata individuals in SE Sweden 2004 2006. y = size year t + 1, x = size year t, z = soil potassium concentration, ppred = proportion of fruits exposed to predation Model component Survival Growth Sample size (n) 1669 1322 1669 625 1345 297 345 92

Value (standard error)

Logit(s) = 1.39(0.31) + 0.49(0.04)x Y = 2.13(0.17) + 0.71(0.02)x + 0.013(0.003)z, 2 = 1.25 Flowering Logit( fp) = 9.90(0.56) + 1.18(0.07)x Fruit number Log( fn) = 0.31(0.19) + 0.28(0.02)x Seed number fs = 0.39ppred + 9.26(1 ppred) Germination pe = 0.0062 Seedling survival ps = 0.24 Seedling size Mean = 3.08, SD = 1.45

effect was statistically signicant in all mixed-effects vital-rate models (Table 2). Environmental factors had signicant effects on vital rates in terms of effects of soil potassium concentration on individual growth rate and of May canopy openness on fruit number. There were no signicant effects of intra- or interspecic density. Judged by comparisons of likelihood ratios between full models and models containing only size (Hosmer & Lemeshow 2000), model t was not much improved by the inclusion of environmental variables (Table 2). This suggests that environmental effects on vital rates were overall relatively small. Seed predation had a large effect on seed number. Attacked fruits contained on average 0.39 intact seeds compared to 9.26 seeds in intact fruits (Table 3). The proportion of fruits exposed to predation was about three times higher in 2005 than in 2004 (0.29 and 0.10, respectively). The proportion of fruits damaged by predation was skewed, with most individuals suffering no losses (Fig. 1). None of the other environmental variables had an effect on the number of seeds per fruit when accounting for predation.

Fig. 1. Proportion of fruits exposed to pre-dispersal seed predation in Actaea spicata individuals in 2004.

Based on the results of the statistical models, we included pre-dispersal seed predation and soil potassium concentration in the IPMs. Both seed predation and canopy openness in May indeed signicantly inuenced the same vital rate, seed production. We chose to include only one of these factors, seed predation, because we wanted to keep models relatively simple and because seed predation had the largest effect (changing May canopy cover from its lowest to its highest observed value resulted in a reduced seed production that was 46% of that resulting from a change in seed predation from the lowest to the highest value). The effect of soil potassium concentration was included in equation 2 as a part of the regression model describing individual growth (Table 3). We assigned each examined potassium level to all individuals. Including the observed intrapopulation variation in potassium had a negligible effect on the results (not shown).

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Fig. 2. Elasticity of population growth rate to fertility and size transitions in Actaea spicata. Transitions go from present size on the x-axis to future size on the y-axis. The diagonal eld corresponds to survival-growth elasticities of established individuals. The bottom right eld corresponds to recruitment (fruit production, probability of seedling emergence and probability of seedling establishment).

Fig. 3. Population growth rate () of Actaea spicata, as a function of soil potassium concentration and level of pre-dispersal seed predation. The largest level of predation (0.57) corresponds to all fruits in primary infructescences being infested by seed predators. The growth rate, with associated 95% condence interval, corresponding to mean observed potassium concentration and mean observed predation is marked.

Observed vital rates in permanent plots corresponded to = 1.010 and the 95% condence interval included 1.0 (0.9941.027). When specifying a model for each year, the two studied transitions represented one year of positive population growth and 1 year of decline; = 1.04 and 0.94, respectively. The stable size distribution predicted by the models agreed reasonably well with the observed distribution and calculated values were similar to observed changes in the number of established individuals (not shown). Elasticity analyses showed that proportional changes in survival-growth transitions of large individuals had the greatest effects on (Fig. 2). Survival-growth elasticities of individuals larger than 8.1 (ln mm3) constituted 68% of the total elasticity. Population growth rate in environments representing different levels of soil potassium and seed predation ranged from below to above 1.0 (Fig. 3). High and low levels of potassium concentration resulted in growth rates falling outside of the 95% condence interval of the observed value of . At the observed mean seed predation level, the lowest and highest observed soil potassium concentrations corresponded to = 0.96 and = 1.07, respectively. At the observed mean potassium concentration, predation of all fruits in primary infructescences and no seed predation corresponded to = 0.987 and = 1.020, respectively. The potential effect of canopy openness in May on growth rate via seed production was weaker; minimum and maximum observed canopy openness in May corresponded to = 1.000 and = 1.017. Elasticity values suggested that a change in potassium concentration should have a larger effect on population growth rate than an equally proportional change in seed predation level (0.069 vs. 0.010).

Discussion
This study illustrates how abiotic and biotic environmental factors can be incorporated into detailed demographic models to assess their relative importance for population growth rate. The results show that variation in soil potassium concentration had the potential to change population growth rate () of A. spicata from positive to negative via a relatively weak association with individual growth rate. Seed predation had a substantial effect on population growth rate and canopy openness in May also inuenced through effects on seed production. According to the statistical and demographic models, potassium had a larger effect on population growth rate than seed predation and plant density, which are likely to be the most important biotic interactions of this plant. Mean population growth rates of long-lived perennial herbs are not expected to deviate much from unity (e.g. Garca et al. 2008; Morris et al. 2008). Still, the growth rates associated in our study with extreme potassium concentrations (range: 0.961.07) and seed predation intensities (range: 0.991.02) may result in large changes in population size over a relatively short time period. For example, over 10 years a population with a growth rate of 0.96 would decrease to 66% of its initial size, whereas a population with a growth rate of 1.07 would increase by 98%. Knowledge of how environmental factors inuence population dynamics of a particular species is often limited. Using regression analyses for estimating environmental effects on vital rates constitutes a way both to identify potentially important factors and to provide an estimate of their potential impact. The use of regression models is particularly appealing

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J. P. Dahlgren & J. Ehrln spicata, however, seedling density is negatively correlated to pre-dispersal seed predation rates (von Zeipel 2007). In addition, in long-time monitoring of seed sowing experiments on this species no compensating mortality in later life stages has been detected (Ehrln & Eriksson 2000). In conjunction with these results, the effect of seed predation on population growth rate in our model thus suggests that plant population growth rate, and therefore habitat range, can indeed be restricted by herbivores. In our study system, the translation of mean individual seed predation rates to effects on population growth rate is also straightforward in the sense that seed predation rates do not depend on the size of the inorescence; the proportion of fruits attacked is independent of the total number of fruits (von Zeipel 2007, but see Rose et al. 2005). The importance of a factor inuencing population growth rate depends both on the magnitude of the effect on vital rates and on the sensitivity of population growth rate to the affected vital rates. In our study, population growth rate was more strongly inuenced by smaller proportional changes in individual growth due to differences in potassium concentration than by larger reductions in seed number caused by seed predation or canopy openness. The larger sensitivity of population growth rate to changes in growth and survival of adult plants than to changes in reproduction is a property that A. spicata shares with many long-lived plants (Silvertown et al. 1993). Short-lived plants, on the other hand, rely more on reproduction. Our results thus stress that to assess environmental effects on populations, we need to integrate information about environmental effects on tness components with information about species life histories, that is, determine the sensitivity of population growth rate to tness components. Environmental effects on population growth rate may also depend on uctuations of environmental factors and on population density. Stochastic variation can be important to include in population models if yearly uctuations are large (Morris & Doak 2002). However, available information suggests that variation in vital rates among years is relatively small in our study system, which seems to be the case also for many other long-lived species in stable environments (e.g. Colling & Matthies 2006; Miller et al. 2007; Morris et al. 2008). Seed predation rates within A. spicata patches, on the other hand, may vary substantially among years and contribute to temporal variation in population growth rate. We found no evidence of effects of intra- or interspecic density on any of the vital rates of A. spicata. Still, density-dependent processes may play a role at higher densities. If negative effects of density are indeed present, then populations may be able to survive in environments characterized by lower potassium concentration and higher seed predation than suggested by simulations. To our knowledge this demographic study is the rst that has incorporated both abiotic and biotic interactions and shown how they can inuence plant population growth rate. Such approaches are important not only because they enable an assessment of the relative importance of factors, but also because they allow the analysis of population dynamics in a more realistic ecological setting. In a spatial context, demographic models that include environmental factors can be used in

since they can be incorporated directly into IPMs (cf. Ellner & Rees 2006). In our study, there are two potential limitations to the interpretations of the results. First, our individual-level estimates of soil characteristics were based on measurements in each plot quadrant rather than at each individual. If the variation among individuals is larger than variation among plot quadrants, then actual effects of soil characteristics are larger than suggested by our model results. Secondly, our study documents correlations between environmental factors and vital rates rather than proving causal relationships. In our study, increases or decreases in mean soil potassium concentration over the observed range were associated with changes in population growth rate of around 5%. As far as the goal is to make predictions of the suitability of a particular environment for a species, demonstrating such a correlation is often sufcient. However, experimental manipulations are needed to corroborate the causal relationship. A previous greenhouse experiment with A. spicata has established an effect of potassium on individual growth (Salomonson et al. 1992), but additional experiments are necessary to conrm effects of potassium in the eld. Few other studies have estimated effects of abiotic factors on plant population growth rate, but Gotelli & Ellison (2002) found that an increase in nitrogen deposition rate of only 1% substantially increased the local extinction risk of the pitcher plant Sarracenia purpurea. The effect of soil potassium found in our study is particularly interesting because concentration of potassium, as well as of other nutrients (Leuschner & Rode 1999), is known to change during forest succession. Potassium concentration may thus be one factor restricting A. spicata to mainly mid-successional deciduous forest in the study area. Pre-dispersal seed predation and canopy openness early in the growing season also had the potential to reduce population growth rates and cause population decline in A. spicata at low soil potassium levels. A more open tree canopy was associated with a higher number of fruits, and therefore seeds, produced per individual. Given that the fruit set in A. spicata is close to 100%, this may have been caused by lower rates of assimilation and fewer resources for fruit production with increasing canopy cover. Over the observed range of the respective factors, seed predation had larger effects on seed production and population growth rate than canopy openness, and reduced the number of seeds per fruit dramatically. The difference in growth rate between populations with no predation and maximum observed seed predation corresponds to a difference in of 0.033. This effect of seed predation is similar to what has been found in previous studies of this species, using different methods (Frborg & Eriksson 2003). For other long-lived perennial plants, reductions in population growth rate caused by seed predation range from 0% to 7.6% (Kolb et al. 2007). A general problem for the interpretation of the effects of seed predation predicted by population models is that reduced seed number may not necessarily translate into proportional reductions in recruitment if seed and seedling mortality rates are density-dependent. This is one reason why the evidence for herbivore-limited population growth rates has been questioned (Halpern & Underwood 2006). In A.

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Linking environment and population dynamics 673 conjunction with niche- or habitat range models (e.g. Guisan & Zimmermann 2000) to delimit suitable habitats for a species. For this use, demographic models are limited by the fact that they are based on environmental data only from within the distribution range, while their strength lies in being more mechanistic and detailed. Incorporating environmental factors in demographic models constitutes a powerful tool to examine population dynamics and population viability also in temporally varying environments. If we have knowledge of how relevant environmental factors are likely to change over time, then these changes can be incorporated in the models and the consequences of temporal environmental change for population dynamics and viability can be predicted.
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Acknowledgements
We wish to thank J. Azali, M. Bengtsson, M. Dahlgren, T. Lund Jrgensen and S. Rosengren for help with the eldwork. We are grateful to E. E. Crone, O. Eriksson, P. A. Hambck, M. Rees and P. A. Zuidema for comments on earlier versions of the manuscript. The study was nanced with grants from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) (to J. E.).

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