Spatial variation in population growth rate and. community structure affects local and regional dynamics

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1 Journal of Animal Ecology 2008, 77, doi: /j x Spatial variation in population growth rate and Blackwell Publishing Ltd community structure affects local and regional dynamics M. Kurtis Trzcinski 1 *, Sandra J. Walde 1 and Philip D. Taylor 2 1 Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1; and 2 Atlantic Cooperative Wildlife Ecology Research Network, Department of Biology, Acadia University, Nova Scotia, Canada B4P 2N5 Summary 1. Theory predicting that populations with high maximum rates of increase (r max ) will be less stable, and that metapopulations with high average r max will be less synchronous, was tested using a small protist, Bodo, that inhabits pitcher plant leaves (Sarracenia purpurea L.). The effects of predators and resources on these relationships were also determined. 2. Abundance data collected for a total of 60 populations of Bodo, over a period of 3 months, at six sites in three bogs in eastern Canada, were used to test these predictions. Mosquitoes were manipulated in half the leaves partway through the season to increase the range of predation rates. 3. Dynamics differed greatly among leaves and sites, but most populations exhibited one or more episodes of rapid increase followed by a population crash. Estimates of r max obtained using a linear mixed-effects model, ranged from 1 5 to 2 7 per day. Resource levels (captured insect) and midge abundances affected r max. 4. Higher r max was associated with greater temporal variability and lower synchrony as predicted. However, in contrast to expectations, populations with higher r max also had lower mean abundance and were more suppressed by predators. 5. This study demonstrates that the link between r max and temporal variability is key to understanding the dynamics of populations that spend little time near equilibrium, and to predicting and interpreting the effects of community structure on the dynamics of such populations. Key-words: maximum rate of population increase, persistence, pitcher plant, predation, population stability, population synchrony, protozoa, temporal variability Introduction Three interrelated parameters are critical to the description of simple or complex local population dynamics: maximum population growth rate (r max ), realized growth rate (r), and density dependence (resource limitation) (Royama 1992; Murdoch 1994; Turchin 2003; Sibly et al. 2005). As r max is simply the difference between per capita birth and death rates in the absence of resource limitation, it often varies across environments, where differing abiotic and biotic conditions lead to different rates of mortality and fecundity. Maximum growth rate (r max ) can thus be thought of as an integrated measure of density-independent effects on birth and death *Correspondence author: Population Ecology Division, Bedford Institute of Oceanography, Department of Fisheries and Oceans, P.O. Box 1006, Dartmouth, Nova Scotia, Canada B2Y 4A2; trzcinskik@mar.dfo-mpo.gc.ca rates, while realized growth rates reflect the impact of resource limitation in addition to density-independent factors. The extent to which maximum growth rate has been reduced (to the realized rate) is thus a measure of the strength of density dependence. It has been argued that population growth rate is a better measure of the state of a population than population size; growth rates can be viewed as a window to the key pressures on a population and be used to elucidate the causes of population dynamics (Hone & Sibly 2002; Sinclair & Krebs 2002). Very different dynamical patterns can emerge as r max or the strength/form of density dependence changes. Early theoretical work demonstrated that population stability was highly sensitive to the intrinsic (maximum) rate of increase; the higher a population s rate of increase, the more likely it is to show complex dynamics (May 1976; Hassell, Comins & May 1976). There is good empirical evidence for cyclic dynamics (Kendall, Prendergast & Bjørnstad 1998), and some evidence 2008 The Authors. Journal compilation 2008 British Ecological Society

2 1154 M. K. Trzcinski, S. J. Walde & P. D. Taylor for chaotic dynamics in natural food webs (e.g. Turchin & Ellner 2000). Large amplitude, apparently irregular fluctuations have been documented for some arthropod (e.g. Solbreck & Ives 2007) and protozoan populations (e.g. Gonzalez & Holt 2002). Species interactions, including parasitism (Hassell 2000; Hudson et al. 2002), predation (Huffaker 1958; Hanski et al. 2001), and competition (Tilman 1994; Long, Petchy & Holt 2007), can lead to instability, especially under conditions leading to high r max. Environmental fluctuations can also produce high amplitude population fluctuations through their effects on r, particularly if the temporal variability in the environment is autocorrelated (Luckinbill & Fenton 1978; Petchy 2000; Gonzalez & Holt 2002; Roy, Holt & Barfield 2005). Population growth rate is also a critical parameter when stability is derived from spatial processes. Dispersal and asynchrony affect the regional stability of locally unstable interconnected populations (Reeve 1988; Harrison & Quinn 1989; Hanski 1999). Recent theoretical work has shown that the degree of synchrony is affected by the rate of population increase, dispersal and environmental correlations (Heino et al. 1997; Ranta et al. 1997; Lande, Engen & Saether 1999; Earn, Levin & Rohani 2000; Kendall et al. 2000), and thus by any factor that affects any of these (e.g. temp, rainfall, predators). In this study, links between population growth rate and dynamics are examined for a key component of the protozoan community (Bodo Ehrenberg) inhabiting pitcher plant leaves (Sarracenia purpurea L.). Local variation in r is first explained in terms of differences in abiotic and biotic factors, and then linked to observed variation in dynamics. The relatively simple community in pitcher plant leaves (aquatic insects, mites, protozoa, rotifers and bacteria) has been used to test many ideas in population and community ecology (Addicott 1974; Cochran-Stafira & von Ende 1998; Kneitel & Miller 2002; Miller, Kneitel & Burns 2002; Kneitel & Miller 2003; Trzcinski, Walde & Taylor 2005a; Gray et al. 2006). The microflagellate, Bodo, is usually the most numerous protozoan, and occupies a central place in the food web, feeding on bacteria, and serving as an important prey for the top predator (mosquito larvae) (Addicott 1974; Cochran-Stafira & von Ende 1998; Kneitel & Miller 2002). Individual populations of Bodo exhibit wide variation in abundance over short time periods and nearby populations can exhibit completely different temporal patterns of abundance. Some variation has been linked to variation in food web structure and some to colonization dynamics (Kneitel & Miller 2002; Miller et al. 2002; Trzcinski et al. 2005a,b) but much remains unexplained. The eruptive dynamics and lack of persistence of many Bodo populations suggest local instability that could be caused by high r, and spatial variation in r is thus one plausible explanation for variation in dynamics across local populations. In this study, 60 populations of the protozoan, Bodo sp., from eastern Canadian bogs, were censused biweekly over 3 months. Partway through the season, mosquito densities were manipulated in half the leaves to increase the range of predation rates. The time series were used to estimate r max for each population, and to test the following predictions: (i) populations with high maximum rates of increase (r max ) will be less stable as measured by persistence and variation in population abundance, and (ii) metapopulations with high maximum rates of increase will be less synchronous. For each prediction, we determine if and how predators and resources alter these relationships. Methods Pitcher plant leaves fill with rain water, are colonized by bacteria, protozoa, rotifers, and arthropods, and passively capture insects and other unfortunate creatures (Heard 1998), which decay and serve as the food resource for the aquatic community and for the pitcher plant. The arthropod community in the study area (44 29 N, 63º32 W) consists of an aquatic mite Sarraceniopus gibsoni Nesbitt, and three larval Diptera: a mosquito, Wyeomyia smithii Coq., a midge, Metriocnemus knabi Coq., and a sarcophagid fly, Blaesoxipha fletcheri Aldrich. Mosquitoes prey on bacteria and protists in the water column, while midges and mites feed on decaying material at the bottom of the leaf. Leaves typically contain a diverse protozoan assemblage (Addicott 1974; Kneitel & Miller 2003), and as in many other communities, most species are rare. In this study, the focus was on the most abundant of the microfauna, Bodo, a small flagellate (5 12 μm). Two sites (35 35 m) were selected in each of three eastern Canadian coastal bogs (Duncan s and Sandy s Cove are 3 1 km apart and are about 27 km from Peggy s Cove). Water samples were collected biweekly from 60 leaves (one leaf from 10 randomly chosen plants at each site) from 6 July to 2 October 2000 (27 sampling dates over 89 days). Leaves were left open to natural colonization. On each visit, water level was measured and three 170-μL samples were collected from each leaf. Bodo density was determined for each sample and total abundance was then estimated using a regression model that included water level and leaf morphology (r 2 = 0 89) (Trzcinski et al. 2005a). On 8 August, after the peak period of mosquito oviposition, mosquito density was manipulated by adding five larvae to half the leaves at each site. On 2 October, leaves were collected, measured (maximum length), and arthropod (mosquitoes, midges and mites) inhabitants were counted. Captured insects (mostly ants) were also counted. Mean daily (24 h) temperature over the 3 to 4 days before each sampling date was calculated from records of daily air temperature obtained from a station located 500 m from the Duncan s Cove bog. Intermittent temperature data were also available for Sandy s Cove, and seasonal trends at the two sites were strongly correlated (r = 0 90, P < 0 001) with Sandy s Cove being ~1 5 C cooler on the warmest days. It was thus assumed that the general trend in mean air temperature over the season was similar among sites and bogs. STATISTICAL ANALYSES The analysis consisted of (i) estimating the maximum rate of population increase (r max ) and determining if r max differed among bogs and sites, (ii) testing for the influence of the insect community and resources on r max, and (iii) testing for the effect of r max on local Bodo population dynamics and on population synchrony within a site. Estimating r max A linear mixed (Gompertz) model, including all 60 time series, was used to estimate the maximum rate of population increase within

3 Spatial variation in population growth rate each leaf (Jacobson et al. 2004; Jonzén et al. 2005). The form of density dependence assumed in the Gompertz model has the rate of increase declining linearly with the log e of population abundance, a form commonly observed in populations with high rates of increase, such as insect populations (Sibly et al. 2005). (The Gompertz model is simply a special case of the theta-logistic model, where θ = 0.) The model was generalized by assuming that parameters for each leaf were random variables nested within site, and a term for temporal variation in temperature was added. Finite changes in population size were standardized by the sampling interval (Δt = 3 or 4 days) and were modelled as y ijk = β 0ij + β 1ij x ijk + b i + b j(i) + β 3 T k + ε ijk, i = 1,... 6, j = 1,... 10, k = 1, where y ijk = log(n k+1 /N k )/Δt, x ijk = log(n ijk ), and i was site, j was leaf, and k was the time interval. This model generalized a linear regression between the finite rate of increase [log(n k+1 /N k )] and population size [log(n ijk )] by specifying leaf within site (b j(i) ) and sites within bog (b i ) as random effects, and population size and air temperature (T k ) as fixed effects. The b i, b j(i) and ε ijk s were assumed to be independent random variables with N(0, σ 2 ). The slope β 1ij estimates the strength of density dependence and the y-intercept β 0ij estimates the maximum rate of increase (r max ) of a leaf at a site. Temporal variation in air temperature was included, as temperatures tended to decrease over the sampling period. Multiple regression was used to determine if the parameter estimates of r max differed among bogs and sites, and to determine which aspects of the community (mosquito additions, natural mosquito colonization, midge and resource abundance) best explained among leaf and among site variation in maximum population growth rate. Effects of r max on local dynamics Multiple regression was used to determine how population dynamics were linked to r max. Abundance was the mean of the 27 abundance estimates over the 89-day time series. Three measures of stability were used, temporal variability, estimated by the coefficient of variation (CV) after correcting for sampling variability, and persistence time (log transformed) measured as the number of sequential sampling dates over which non-zero abundances were obtained. A population was deemed extinct if no individuals were obtained in any sample over three consecutive sampling dates (details in Trzcinski et al. 2005a). Degree of resilience, or ability to track changing resource levels, was estimated as the Pearson correlation coefficient for the relationship between Bodo and bacterial abundances over time within each leaf (without a time lag, and with a lag of one sampling period; 3 days). Bacterial abundances were placed into one of five density categories: none, low, medium, high, and extremely high (0, 1 5, 6 99, , >500 cells per μl of concentrated fluid) (details in Trzcinski et al. 2005a). Effects of r max on synchrony Population synchrony was estimated as the pairwise Spearman s rank correlation coefficient for Bodo abundances over time for all possible pairwise combinations of leaves within each site (10 10 matrix). Regional synchrony for the site was then calculated as the mean of all unique pairs (Bjørnstad, Ims & Lambin 1999). The deviances from mean abundance for all leaves within a site were plotted against time (Cazelles, Bottani & Stone 2001) to identify synchronizing or desynchronizing events; synchronizing events cause the lines to converge to zero, whereas desynchronizing events cause divergence. Linear regression was used to test for a relationship between pairwise synchrony and distance between leaves, within sites (maximum distance 35 m) and within bogs (maximum distance 240 m). Lastly, the link between site-level r max and synchrony was tested in a general linear model with r max and the mean abundance of mosquitoes and midges as explanatory variables. All analyses were conducted in s-plus version 6 2. Results Local Bodo populations displayed a wide variety of dynamical patterns, and the timing, magnitude and number of peaks varied among populations within a single site (Fig. 1) and among sites, with abundances generally highest during the first half of the season and declining through the fall (Fig. 2). Temporal variability of individual populations was high; CV at the site level ranged from 1 0 to 1 7, while individual populations had CVs as high as 6 8. Only 8 of 60 leaves were persistent for the entire sampling period. VARIATION IN R MAX The maximum population growth rate, r max, for all Bodo populations considered jointly, was 2 03 per day (0 20 SE, P < ), corresponding to a doubling time of about 8 h in the field. Individual populations had values of r max ranging from values of 1 52 to 2 73 per day (Fig. 3). Most populations grew quickly in early July, and declined rapidly in mid-july to early August. Rates of increase depended mostly on population density (i.e. density dependence; slope = ± SE, P < ). Temperature had a small, positive effect on r max (slope = ± SE, P = 0 04); an increase of 1 C caused individuals to produce approximately 10 more offspring per day. There was more variation in r max between sites within a bog than among bogs; the lowest (1 53), and highest (2 73) r max occurred in two sites from the same bog (Peggy s Cove). Among-bog and among-site variation explained significant proportions of the variation in r max (variance components: total sum of squares (SS) = 4 39, bog SS = 0 57, site SS = 1 73). Population growth rate differed among sites, and was affected by resources and midges, although the effects were present only at some sites (Table 1). While the mosquito manipulation did not significantly affect r max directly (P = 0 10), it did alter the effect of midges on r max, changing the relationship from positive in unmanipulated leaves (mosquitoes present in low numbers due to natural colonization), to negative for leaves where mosquitoes were added (Table 1). The highest values of r max were seen at Peggy s Cove (which we assume to be the coolest bog given its proximity to the ocean) indicating that site-level differences were not likely driven by temperature. Seasonal variation in temperature was included in the model estimating r max.

4 1156 M. K. Trzcinski, S. J. Walde & P. D. Taylor Fig. 1. Variation among leaves in the dynamics of Bodo. Data are abundance by sampling date for four populations from site 1 (Duncan s Cove) from 6 July to 2 October. Error bars are 1 SE. Fig. 2. Variation in the population dynamics of Bodo among sites. Each line is the mean of ten leaves. Duncan s Cove, sites 1 and 2; Sandy s Cove, sites 3 and 4; Peggy s Cove, sites 5 and 6.

5 Spatial variation in population growth rate Table 2. Results of models testing for the effects of r max and community structure on mean abundance, temporal variability (CV), persistence and tracking ability of Bodo populations. Tracking was measured as the correlation between Bodo and bacterial abundance d.f. Sum of squares F-value P value Fig. 3. Variation among sites in estimates of maximum population growth rate (r max ). Box plots indicate the median (line), interquartile range of the data (box), tails of the distribution (bars = 1 5 interquartile range), and outliers (points). Table 1. Results of model testing for effects of the insect community and resources on variation in r max among populations (leaves) within sites EFFECT OF R MAX ON POPULATION DYNAMICS AND SYNCHRONY Coefficient d.f. Sum of squares F-value P-value Null Trt Site < Mosq Midge Resource Trt mosq Trt midge Trt resource Site mosq Site midge Site resource Trt, mosquito manipulation; mosq, mosquitoes colonizing leaves; midge, midges colonizing leaves; resource, captured insects. There were significant relationships between r max and several aspects of local Bodo population dynamics. In contrast to expectations, populations of Bodo with higher r max had lower mean abundance, both before (P = 0 002, coefficient = 2 55) and after the mosquito manipulation (P = 0 02; coefficient: 3 69) (Table 2, Fig. 4). Abundances of Bodo were also much lower where mosquitoes were added, and the negative effect of mosquitoes was greater for populations with higher r max. Populations with higher r max showed greater temporal variation (CV) in population abundance over the entire sampling period (P = 0 004) (Table 2, Fig. 4), although r max Mean abundance (post-mosq. manip.) Null Trt Bog Site r max Mosq Midge Resource Trt r max CV (entire time) Null Trt Bog Site r max Mosq Midge Resource CV (post-mosq. manip.) Null Trt Bog Site r max Mosq Midge Resource Trt r max Persistence (entire time) Null Mean abundance Trt Bog Site r max Mosq Midge Resource Trt r max Tracking of bacteria (entire time) Null Trt Bog Site r max Mosq Midge Resource Trt r max Trt, mosquito manipulation; mosq, mosquitoes colonizing leaves; midge, midges colonizing leaves; resource, captured insects. was unrelated to persistence times (P = 0 68). Population with higher r max also did not track changing resources more closely than did slower growing populations (P = 0 43) (Table 2, Fig. 4). All temporal correlations between Bodo

6 1158 M. K. Trzcinski, S. J. Walde & P. D. Taylor Fig. 4. Relationships between four measures of population dynamics and maximum population growth rate (r max ). Mean population abundance (a), temporal variability (CV) (b), population persistence (c), and the correlation between Bodo and bacterial abundance. Fig. 5. The relationship between population synchrony (residuals after accounting for variation in mosquito and midge abundance) and maximum population growth rate (r max ). Numbers indicate site, Duncan s Cove, sites 1 and 2; Sandy s Cove, sites 3 and 4; Peggy s Cove, sites 5 and 6. abundance and bacterial density within a leaf over time were positive, and half (30/60) were significant at P < 0 05 (8/60 at P < , Bonferroni correction), with Pearson coefficients ranging from to The number of significant relationships between Bodo and bacteria did not increase when tested at a lag of one sampling date (3 or 4 days). Bodo dynamics were strongly affected by the mosquito manipulation. Where mosquitoes were added, Bodo abundances were lower, temporal fluctuations were greater, persistence was lower (Table 2), and there was a tendency for better tracking of fluctuations in bacterial density (P = 0 08). In addition, the relationship between r max and temporal variability was gone after the mosquito manipulation (corresponding to the period of mosquito residence in the leaves). Resources tended to have a positive effect on Bodo abundance (P = 0 07, Table 2), but the effect size was small, and resources were unrelated to temporal variability or persistence. There was also considerable variation across sites in the degree to which local populations were synchronized. Populations at sites that had higher average mosquito and midge abundances were less synchronized. While the simple correlation between site-level synchrony and r max was not significant (slope = 0 48, P = 0 33), inclusion of mosquito and midge abundance in a general linear model resulted in a significantly negative relationship between site level r max and population synchrony (Fig. 5; r max : ± 0 17 SE, P = 0 03; mosquito: ± SE, P = 0 04; midge: ± SE, P = 0 07). Nearby populations were not more synchronized than distant populations. Synchrony did not decline with distance at any site (P > 0 26), nor was there a site-by-distance interaction (P = 0 23). Rainfall appeared to induce some synchrony at some sites; plots of individual deviations from the site means over time showed weak tendencies for convergence (increased synchrony) for some rainfall events at several, but not all of the sites (Fig. 6). Discussion Populations with higher r max showed larger fluctuations in abundance, as predicted by models ranging from the simple

7 Spatial variation in population growth rate Fig. 6. Within-site coherence in the dynamics of Bodo population. Each line represents the deviation in abundance of an individual population (x i ) from the site average. Arrows indicate rain events, and the dotted line shows the timing of the mosquito manipulation. Lines converging to zero indicate an increase in synchrony within the metapopulation. Duncan s Cove, sites 1 and 2; Sandy s Cove, sites 3 and 4;, Peggy s Cove, sites 5 and 6. time-lagged logistic to more complex food-web models (May 1976; Hassell 1978; Hassell 2000; Hudson et al. 2002). Local Bodo populations showed little evidence of being at equilibrium in this study, even over short time periods. Most populations had one or more episodes of rapid increase followed by even more rapid crashes (Fig. 1). Temporal fluctuations were large, with maximum to minimum ratios of over 3000 (excluding zeroes) and up to sevenfold declines over single sampling intervals (3 days). Extinctions were the norm; Bodo went extinct at least once in 23/30 unmanipulated leaves and in 29/30 leaves where mosquitoes were added. Stable equilibria may not be the norm for many pitcher plant microfauna; Addicott (1974) found a decline in species richness over time, implying extinctions, and Kneitel & Miller (2003) showed that dispersal can have an important rescue effect. The upper ranges of the r max estimates (1 5 to 2 7 per day) are high enough to produce large amplitude cycles in simple logistic models with time lags (τ 1). The imperfect tracking of bacterial abundance by Bodo populations suggests the presence of such time lags, although our sampling interval of 3 days precluded checking for lags at the scale of single generations. The various indirect interactions documented in other pitcher plant communities (from apparent competition to trophic cascades) may also contribute to lagged responses. Thus, the high observed population growth rates, the large and irregular fluctuations in abundance, and the increase in amplitude of fluctuations in populations with higher r max, all suggest that Bodo dynamics are not well characterized by a stable equilibrium set by resource levels. The dynamics of Bodo populations in pitcher plant leaves were highly variable, with populations often remaining at low densities for long periods and then outbreaking to very high densities. This type of population dynamic is not uncommon in forest and agricultural insect pests, and longer time series indicate that it may be characteristic of more systems than previously thought (e.g. Ferriere & Cazelles 1999, Yoshida 2005). Recent advances in theory, as well as some empirical tests, demonstrate that autocorrelated environmental signals can lead to high amplitude, irregular fluctuations and extinction, although persistence is possible with dispersal (e.g. Morales 1999; Petchy 2000; Gonzalez & Holt 2002; Holt, Barfield & Gonzalez, 2003; Pike et al. 2004; Roy et al. 2005; Matthews & Gonzalez 2007). This mechanism produces dynamics that resemble those seen for Bodo, an outbreak to high density when a string of good days occurs, and then a rapid decline, followed by extinction, or a long period of low densities. Seasonal temperatures are strongly autocorrelated, and their

8 1160 M. K. Trzcinski, S. J. Walde & P. D. Taylor effects on resource capture and breakdown rates are also likely to show autocorrelation. The dynamics of Bodo populations are largely internally driven (Cochran-Stafira & von Ende 1998; Kneitel & Miller 2002; Trzcinski et al. 2005a), and variation in the composition of the local community probably contribute to the variation among populations in timing of the high amplitude fluctuations. Most outbreaks occurred early in the season, before mosquito colonization, suggesting that mosquitoes likely limit the potential of Bodo to take advantage of favourable environmental conditions. The maximum rate of increase of a population can be thought of as a summary variable, reflecting the summed effects of many environmental factors on birth and death rates. Resources appear to be of major importance in determining maximum rates of increase for Bodo. Higher levels of resources were associated with higher maximum growth rates; at several sites, growth rate increased with pitcher capture rate, while at other sites, the strongest relationship was with midge abundance. Midges affect the rate of breakdown of captured insects, and thus are likely to enhance resource availability (Heard 1994). A curious result was the influence of the mosquito manipulation on the midges Bodo growth rate relationship: a positive effect was seen for unmanipulated populations, but a negative relationship emerged for populations where mosquitoes had been added. Mosquito larvae are known to grow faster in the presence of midges (Heard 1994). Mosquitoes were added to increase the range of observed predator densities, and thus a possible interpretation is that Bodo experiences higher mortality in pitchers with faster growing, and presumably larger mosquito larvae. Rates of increase varied among sites in addition to effects due to variation in resources, midges and mosquitoes. We suspect that subtle differences in microclimate (shading, temperature, etc.) were responsible for much of this variation. Sites with higher average r max (and more mosquitoes and midges) tended to have populations that were less synchronized. High growth rates can increase the independence of local dynamics if r max is sufficiently high so as to induce complex dynamics, and thus enhance stability at the metapopulation scale (e.g. Allen, Schaffer & Rosko 1993). The degree to which the dynamics of local populations are synchronized is usually determined by dispersal and/or by a common response to environmental change (Ripa 2000; Fontaine & Gonzalez 2005); growth rates can modify the influence of both. Higher growth rates reduce the synchronizing effects of dispersal, as the influence of a few dispersers will be lower (Heino et al. 1997; Ranta et al. 1997; Lande et al. 1999; Earn et al. 2000; Kendall et al. 2000). Patterns and natural rates of dispersal by Bodo among pitcher plant leaves in bogs are not known, but the absence of a synchrony distance relationship suggests low numbers of dispersing individuals relative to local growth rates. Rates of establishment may be especially low in the presence of mosquito predators (Miller et al. 2002). In contrast, high growth rates should increase synchrony through a common response to environmental change (e.g. better tracking of fluctuating resources; Luckinbill & Fenton 1978), unless growth rates are already in the chaotic range. Populations of Bodo with higher r max did not track fluctuations in bacterial density more closely, and neither did they appear to respond more strongly to rainfall or temperature. Thus, the lower degree of synchrony seen at sites with higher average r max is more likely due to increasingly independent dynamics as a result of higher maximum growth rates, and/or the lowered effectiveness of dispersal as a synchronizing force with high r max. Synchrony was also lower at sites with high numbers of mosquitoes and midges. The effect of mosquitoes was opposite to the synchronizing effect seen and postulated for wide-ranging predators (Myers 1998; Ims & Andreassen 2000; Korpimäki et al. 2005). Both mosquitoes and midges have strong effects on local dynamics (Addicott 1974; Heard 1994; Kneitel & Miller 2002; Trzcinski et al. 2005a), and variation in mosquito and midge abundance as well as variation in the time of colonization among local populations probably contributed to the more independent dynamics seen at these sites. To the degree that asynchrony influences regional persistence (Hanski 1999; Earn et al. 2000), variation in local dynamics due to higher r max and higher predation rates ought to lead to greater stability at the scale of sites or bogs. This study has thus shown that variation in local population growth rate (r max ) affects both local and regional dynamics of Bodo populations in a field setting. Maximum growth rates were affected by environmental factors, including temperature and resource availability. Key effects of higher population growth rates were lower average abundance, greater temporal variability and larger predator impacts. The non-intuitive results for average abundance and predator impact were probably due to the large amplitude fluctuations shown by Bodo populations. This has implications for attempts to predict the consequences of the many types of environmental change likely to influence r max, that is, populations and predator prey systems that spend little time near equilibrium may respond quite differently to changes in climate or resources. The links between population synchrony, r max and community structure also have important implications. Lower synchrony with higher local r max has been predicted by theory, but has not been demonstrated in the field; the generality of this effect has consequences for the stability of spatially structured populations. That predators would reduce rather than enhance synchrony was also unexpected, and the circumstances under which this effect is most likely to occur needs to be explored (e.g. generalist feeding habit, predators that cause local extinctions, prey with less stable dynamics). Acknowledgements We thank Mark Johnston, Diane Srivastava, Lenore Fahrig, and two reviewers for comments on the manuscript, Sarah Robertson, Megan Bain and Leah Gerber for technical assistance, and Wade Blanchard and Dan Kehler for statistical advice. This research was supported by a NSERC research grant to S.J. Walde, by Dalhousie University, and by the Dr. Patrick Lett fund. References Addicott, J.F. (1974) Predation and prey community structure: an experimental study of the effects of mosquito larvae on the protozoan communities of pitcher plants. Ecology, 55,

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