of multispecies predator prey interactions

Transcription

1 Ecology , Habitat shape, metapopulation processes and the dynamics Blackwell Publishing Ltd of multispecies predator prey interactions JAMES C. BULL*, NICOLA J. PICKUP*, MICHAEL P. HASSELL* and MICHAEL B. BONSALL* *Division of Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK; Institute of Zoology, Zoological Society of London, Regent s Park, London NW1 4RY, UK; and Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Summary 1. The effects of habitat shape, connectivity and the metapopulation processes of persistence and extinction are explored in a multispecies resource consumer interaction.. The spatial dynamics of the indirect interaction between two prey species (Callosobruchus chinensis, Callosobruchus maculatus) and a predator (Anisopteromalus calandrae) are investigated and we show how the persistence time of this interaction is altered in different habitat configurations by the presence of an apparent competitor. 3. Habitat structure has differential effects on the dynamics of the resource consumer interaction. Across all habitat types, the pairwise interaction between C. chinensis and A. calandrae is highly prone to extinction, while the interaction between C. maculatus and A. calandrae shows sustained long-term fluctuations. Contrary to expectations from theory, habitat shape has no significant effect on persistence time of the full, threespecies resource consumer assemblage. 4. A stochastic metapopulation model for a range of habitat configurations, incorporating different forms of regulatory processes, highlights that it is the spatially explicit population dynamics rather than the shape of the metapopulation that is the principal determinant of interaction persistence time. Keywords: Anisopteromalus, apparent competition, Callosobruchus, extinction, host parasitoid interaction, population dynamics, time-series, regulatory process, spatial arrangement Ecology (006) 75, doi: /j x Ecological Society Introduction Spatial heterogeneity and habitat structure has wideranging ecological implications, from the persistence of infectious diseases (Hagenaars, Donnelly & Ferguson 004) through to the design of nature reserves (Etienne & Heesterbeek 000). Both theoretical and empirical studies of spatial structure have progressed from simply proposing that spatial mechanisms might increase the persistence of ecological systems (Nicholson & Bailey 1935; Wright 1940; Huffaker, Shea & Herman 1963; Pimentel, Nagel & Madden 1963) to quantitative investigations of the effects of metapopulation structure on single species (Levins 1969; Hanski 1991; Hanski 1999), Correspondence: Dr Mike Bonsall, Department of Zoology, University of Oxford, South Parks Road, Oxford, Oxon. OX1 3PS, UK. Tel: ; Fax: michael.bonsall@zoo.ox.ac.uk pairwise interactions (Holyoak & Lawler 1996; Ellner et al. 001; Bonsall, French & Hassell 00) and multispecies assemblages (Forbes & Chase 00; Chase & Ryberg 004; Bonsall et al. 005). Although it is now relatively well established that metapopulation structure has important implications for the dynamics and persistence for a range of ecological scenarios (Hanski & Gaggiotti 004), a remaining challenge is to explore the effects of habitat connectivity, patch arrangements and patch dynamics on the metapopulation processes of persistence and extinction. While there is a considerable body of theoretical work suggesting that habitat shape and spatial heterogeneity is of importance in determining the outcome of resource consumer interactions (Holyoak 000; Snyder & Chesson 003; Amarasekare 004; Jonzén, Wilcox & Possingham 004), the effects of regional spatial heterogeneity on the persistence of more complex ecological interactions are often unclear (Hagenaars et al. 004). In particular, how

2 900 J. C. Bull et al. spatially variable habitats affect local and regional ecological processes such as predator prey interactions, resource consumer dynamics and indirect species interactions remains largely unexplored. Previously, using predator prey metapopulations, it has been shown that large scale spatial structure can affect the persistence of these extinction-prone resource consumer interactions (Holyoak & Lawler 1996; Ellner et al. 001; Bonsall, French & Hassell 00; Bonsall & Hastings 004). More recently, this effect has been extended to show how metapopulation structures and spatial scale can influence the outcome of more complex multispecies interactions (Bonsall et al. 005). By exploring the effects of apparent competition (where two species that do not compete for resource, share a common natural enemy), it has been illustrated that spatial structure can mitigate the ecological effects of this indirect interaction. Four conditions for metapopulation persistence (e.g. Hanski 1999) have been shown to underpin these multispecies interactions. First, single patches are capable of supporting host populations in the absence of parasitoids. Secondly, patches are at high risk of extinction in the presence of parasitoids. Thirdly, there is asynchrony across space and through time between patches, and finally there is rescue of extinct patches (Bonsall et al. 005). Here, we extend this theme to explore how habitat shape influences the persistence and dynamics of resource consumer metapopulations. Using replicated laboratory microcosms we investigate the effects of parasitism (pairwise resource consumer interactions) and shared parasitism (apparent competitive interactions) over a wide range of habitat designs. Metapopulation shapes are varied in the degree of connectivity (number Ecological Fig. 1. Schematic Society, diagram showing the nine spatial arrangements of patches used. Journal Designs of a d Animal alone were constructed as laboratory experimental treatments, while all Ecology, configurations 75, were included in the stochastic process models. See Table 1 for details of mean and variance in connectivity between patches. of links between patches vary but total number of patches is constant). We illustrate that the effects of apparent competition on the persistence time of the multispecies interaction are observed over the full range of habitat designs. Moreover, while habitat shape affects the population dynamics and regulatory processes of the resource consumer interaction, contrary to expectation the shape of the habitat has no effect on the persistence time of either the pairwise or apparent competitive assemblages. Having demonstrated the importance of habitat shape on population dynamical processes, we further explore metapopulation persistence and habitat shape through the development of a number of stochastic population models incorporating differing regulatory processes and embedding these within an expanded range of patch configurations. These hypothetical habitat designs vary in more than just the variance of connectivity, with both the mean number of connections and the maximum distance across the metapopulation being explored. Across all habitat shapes tested, we find that it is the population regulatory processes, not the spatial arrangement of patches which affects persistence time. Materials and methods EXPERIMENTAL DESIGN Laboratory microcosms were used to explore the hypothesis that habitat shape affects the persistence of an apparent competition interaction between the bruchid beetles, Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) and C. chinensis (L.) (Coleoptera: Bruchidae), mediated through parasitism by the parasitoid, Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae). Clear, plastic boxes ( mm) were used as the baseline patch for the study. Patches had a hole (4 4 mm diameter) placed in each of their four sides which could either be blocked or lengths (50 mm) of plastic tube inserted to connect patches horizontally into lattice arrangements of various designs. A single-layer lattice of these patches was used for treatments that included only one bruchid species. In the treatments including both bruchids, patches were stacked into double-layer systems. In these cases, top- and bottom-layer patches were connected by a 5 mm-diameter mesh-covered hole. The mesh (hole size: mm) prevented vertical movement by bruchids and, consequently, any direct, interspecific resource competition. However, this tested experimental design did not inhibit the foraging activity of the parasitoid over both bruchid species and allowed an apparent competitive interaction to be established. Four different experimental arrangements of nine patches were assembled (Fig. 1a d) in which the mean connectivity was constant (mean connections per patch = 1 78) but the variance in connectivity differed [variance of connectivity: line (treatment 1) = 0 194, I-design (treatment ) = 0 694, cross (treatment 3) = and

3 901 Multispecies metapopulation dynamics double-star (treatment 4) = 1 694]. Three different species combinations were established in each of the habitat designs: C. maculatus with A. calandrae and C. chinensis with A. calandrae as separate, two-species interactions and the full, three-species, apparent competition interaction (C. maculatus C. chinensis A. calandrae). All treatments were replicated four times. Experiments were seeded over a period of 3 weeks by introducing three black-eyed beans [Vigna unguiculata (L.) Wapl. (Leguminosae)] and four pairs of bruchids into every patch each week. In the cases of double-layer lattices, two replicates of each treatment were seeded with four pairs of C. maculatus on the upper lattice and four pairs of C. chinensis on the lower lattice, and two replicates the other way around. On the fourth week, a further three beans were placed in each patch (three on each level of double-layer patches) and new bruchids emerged from the beans introduced in week 1. Subsequently, bean resources were replaced following a 4-week resource renewal scheme, with the oldest three beans being replaced from each patch every week. Removed beans were stored for a further 4 weeks and any newly emerging animals were released back into the appropriate patch. After the host species had become established for several generations without dispersal between patches, dispersal for h each week was initiated. This length of dispersal window has been shown previously to result in a significant increase in interaction persistence time compared to unlimited dispersal (Bonsall et al. 005). Parasitoids were introduced after a further two host generations. Four pairs of wasps were introduced over consecutive weeks into three different patches in the metapopulations. Time-series for all species were obtained by counting both alive and dead insects each week from every patch (dead insects were then removed). All experiments were undertaken in controlled environmental conditions (30 C, 70% relative humidity, 16 : 8 light : dark cycle). METAPOPULATION PROCESSES Asynchrony in the dynamics between patches was investigated through spatiotemporal semivariograms for each metapopulation (of n patches), which were calculated using γ( d, τ) = 1 / i= 1 y= 1( xi τ n n xj τ) where x is the individual species, patch specific growth rate for equally weighted time-point τ and spatial reference point (Legendre & Legendre 1998). This statistic categorizes the squared differences in population growth rate between all possible pairs of patches into groups according to the minimum number of steps (d) between the ith and jth patch in the metapopulation. Means, γ (d,τ), for each of these distance categories represent the level of asynchrony and are presented for each distance (d) and time-point (τ). The potential for extinct patches to be recolonized was determined by calculating the conditional probability that a patch, in which a given species was absent at time τ, was subsequently recolonized. Adults had to be absent from any given patch for 4 weeks continuously in the case of hosts or weeks continuously in the case of parasitoids, in order to allow for any developing insects to emerge as adults. This ensured that immigration from neighbouring patches was the only possible source of insects present in patches from which they were found to be extinct. DYNAMICS AND PERSISTENCE To test the hypothesis that habitat structure affects the dynamics of the predator prey assemblage we explore, using analysis of covariance (with population density as a continuous variable and habitat shape as a categorical variable), how the regulatory processes operating in the persistent, pairwise, host parasitoid (C. maculatus A. calandrae) interaction differ between habitat types. We use conventional population ecological analysis of regressing net reproductive rate [ln(n t+1 /N t )] on lagged population density (Royama 199) and include habitat shape as a covariate. Metapopulation persistence times for the pairwise (C. chinensis A. calandrae) and apparent competitive (C. chinensis C. maculatus A. calandrae) interactions were compared using survival analyses (Cox & Oakes 1984) and any replicates persisting at the end of the experiment were censored. Model simplification (stepwise elimination of non-significant explanatory variables) was used to determine the most appropriate, minimal adequate model (the model retaining only significant terms) with residual errors for this survival regression described appropriately by a Weibull distribution. POPULATION MODELS Further investigation of the relationship between dynamical processes and habitat shape were conducted through development and analysis of population simulation models applied to an expanded range of patch configurations (Fig. 1a i). Patch-specific, population dynamics were modelled by using stochastic population models. In particular, autoregressive processes were used to describe time-lagged density-dependent processes (e.g. N i,t, N i,t 1 ) while moving average processes were used to describe density-independent processes (e.g. Z i,t ). For instance, dynamical changes in the ith patch driven by a second-order density-dependent process [AR()] and a first-order moving average process [MA(1)] are described by (Bonsall et al. 00): N = f( N, N, Z, ) it, + 1 it, it, 1 it, εt where f( ) is the underlying stochastic process and ε t is a independent, identically distributed random variable. Three different population dynamic scenarios operating at the patch-level were considered: a first-order density-dependent process [AR(1)], a second-order density-dependent process [AR()] and a secondorder density-dependent process coupled to a first-order

4 90 J. C. Bull et al. Fig.. Representative time-series from the four different habitat arrangements for the three different predator prey interactions: (a d) Callosobruchus maculatus A. calandrae (mean host abundance); (e h) C. chinensis A. calandrae (mean host abundance); and (i l) C. chinensis C. maculatus A. calandrae. As predicted by the P* rule, Callosobruchus maculatus persists in the metapopulation while C. chinensis is the species that is always driven extinct in the apparent competitive interaction see text for further details (solid grey line: C. maculatus; solid black line: C. chinensis; dashed black line: A. calandrae). density-independent process [AR()MA(1)]. Net changes in abundance within the ith patch are also influenced through dispersal: Nit, + δ = ( 1 δi) Ni + λijn where δ i is the density-independent dispersal fraction from the ith patch, N i and N j are the numbers of animals in the ith and jth patch and λ ij is the connectivity matrix that determines the possible links between patches (and allows the effects of different habitat shapes to be explored). In the analysis, habitat shape and regulatory form were considered as separate, categorical variables explaining variance in persistence time. All analyses were completed in S-PLUS. RESULTS p j= 1 In Fig., we show representative time-series from each of the (replicated) pairwise interactions (C. chinensis A. calandrae, C. maculatus A. calandrae) and the apparent competitive interaction (C. chinensis C. maculatus A. calandrae) from the different habitat shapes. Across all habitat types, all replicates of C. maculatus A. calandrae persisted over the course of the experiment ( 3 weeks). We use these time-series to explore how habitat shape affects (meta)population dynamics of the resource consumer interaction. In the apparent competitive j interaction, C. chinensis is always the species that is driven to extinction (Fig. i l). To explore the hypothesis that habitat type and assemblage complexity affect persistence and metapopulation processes we make comparisons between this pairwise interaction (C. chinensis A. calandrae) and the full three-species apparent competitive interaction. METAPOPULATION PROCESSES Testing the hypothesis that asynchrony is affected by spatial and temporal processes reveals that correlations in patch-specific population growth rates are highly variable across space and through time. Temporally explicit variograms of the full three-species interaction and the pairwise C. chinensis A. calandrae metapopulations illustrate that asynchrony increases with distance between patches and varies widely over time (Fig. 3). The highly variable nature of the asynchrony over time masks any clear differences between treatments. However, the parasitoid appears to be more in phase among patches in the two species C. chinensis A. calandrae interaction than in the apparent competition assemblage (Fig. 3). To determine the recolonization potential and rescue of extinct patches, conditional probabilities were calculated for the re-invasion of each of the species in the apparent competitive interaction (Table 1). While

5 903 Multispecies metapopulation dynamics Fig. 3. Semi-variograms of asynchrony in patch-specific growth rate. Representative replicates are shown for all four habitat shapes, top row of four semivariograms shows asynchrony between C. chinensis within apparent competition assemblages, second row shows A. calandrae from the same replicates, third row shows C. chinensis from within two-species assemblages, with the bottom row showing A. calandrae from the same replicates. Measures of n n asynchrony were made using γ( d, τ) = 1 / i= 1 j= 1( xi τ xj τ) see text for further details. all three species in the study show the potential for recolonization, the rate of recolonization varies between species and amongst habitat arrangement (Table 1). Parasitoids demonstrate the greatest frequency of recolonization, followed by C. maculatus, which was the superior apparent competitor in all cases. Recolonization by C. chinensis into patches where it was extinct was rare and in some cases did not occur at all. DYNAMICS AND PERSISTENCE The average abundance (with standard errors), across all habitat shapes, of C. chinensis in the presence of the wasp (A. calandrae) was (5 33) and the abundance of the parasitoid was 5 69 (0 91). In comparison, the abundance of C. maculatus was ( 15) and the abundance of A. calandrae was 38 9 ( 18). The C. chinensis A. calandrae interaction was extinction prone and persists for only about 17 weeks (mean persistence time 17 0 ( 11) weeks). In contrast, the dynamics of the C. maculatus A. calandrae interactions showed sustained long-term fluctuations across all habitat shapes (Fig. 1a d). Differences in temporal density-dependence occur in this resource consumer interaction among the different habitats (Fig. 4): regression of the net reproductive rate vs. lagged population density shows that the dynamics of C. maculatus (in the presence of A. calandrae) are described by different density-dependent relationships (Fig. 4). In particular, model simplification reveals that the dynamics in the two habitats with low variance in connectivity ( line and I-design ) are described by the same density-dependent relationship, whereas separate relationships are required for each of the two other habitats (with higher variance in connectivity, cross and double-star ) (population size habitat shape interaction F,499 = 3 16, P = ).

6 904 J. C. Bull et al. Table 1. Connectivity and species-specific patch recolonization potentials for three species, apparent competition assemblages in nine spatial arrangements of nine-patch habitats Habitat shape treatments Connectivity Recolonization probability Mean Variance Maximum steps across habitat C. chinensis C. maculatus A. calandrae 1 ( line ) ( I-design ) ( cross ) ( double-star ) ( long cross ) Simulated populations 6 ( open Union Jack ) Simulated populations 7 ( ring ) Simulated populations 8 ( square ) Simulated populations 9 ( closed Union Jack ) Simulated populations Fig. 4. Regional population net-reproductive rate vs. lagged density for Callosobruchus maculatus in the different habitat shapes. (a) the regulatory processes in the low variance treatments ( line and I-design ) can be described by the same line while (b c) in the higher variance treatments (b = cross, c = double-star ), the regulatory processes are described by different regression lines. (open circles: cross treatment; solid circles: double-star treatment; grey circles: line and I-design treatments). Overall, in the nine-patch metapopulations, the presence of an apparent competitor (C. maculatus) affected the persistence of the multispecies assemblage (threespecies persistence time: mean = (SE = 1 46) weeks; two-species persistence time: mean = 17 0 (SE = 11) weeks). The distribution, skew and kurtosis for persistence times for the pairwise and apparent competitive interactions in the different habitats are shown in Fig. 5. Mean (SE) persistence times (in weeks) for the pairwise (C. chinensis A. calandrae) interaction were 16 5 (1 7), 17 5 (4 99), 0 33 (5 89) and (5 43) for each of the habitat types (see Fig. 1a d for patch arrangements). Similarly, persistence times for the apparent competitive interaction were (3 59), 10 5 (1 04), 16 5 (4 17) and 13 0 ( 7) for each of the habitat types (Fig. 1a d). Model simplification revealed that the only significant determinant on persistence time was the presence of the apparent competitor (C. maculatus). Across all habitat treatments, there was a statistically significant decrease in metapopulation persistence time due to presence of the apparent competitor ( = 4 048, P = 0 044). Despite almost an order of magnitude range in the variance of connectivity between the habitat shapes and differences in the metapopulation processes (asynchrony and recolonization in individual patches) operating in these different habitats, there was no significant difference in persistence time of the pairwise and apparent competitive predator prey assemblage between spatial arrangements ( χ 1 = , P = 0 994). There was also no significant interaction effect between assemblage type (pairwise, apparent competitive) and habitat shape on metapopulation persistence time ( χ = 3 766, P = 0 15). Stochastic process models incorporating different forms of temporal autocorrelation were used to investigate further the relationship between habitat shape and population regulatory processes. Across all patch arrangements, habitat shape had no significant impact on persistence time (F 8,133 = 0 78, P = 0 666). However, regulatory process did have a significant effect on persistence time (F,133 = , P < 0 001) (Fig. 6). χ 1

7 905 Multispecies metapopulation dynamics Fig. 5. Box whisker plots showing the distribution, skew and kurtosis of metapopulation persistence times for (a) the pairwise interaction between C. chinensis and A. calandrae and (b) the apparent competitive interaction. The central line in each box shows the median time to extinction (in weeks), with the box extending to cover the interquartile range and whiskers extending to 1 5 times the interquartile range (habitat treatment codes are 1 = line, = I-design, 3 = cross and 4 = double-star ). Under AR(1) processes, the mean persistence time (1 98) of the metapopulation systems was significantly longer than persistence under an AR() or an AR()MA(1) process (5 74, 5 9, respectively). Discussion Here we have evaluated the metapopulation processes in a multispecies host parasitoid assemblage. We have shown that the presence of an apparent competitor can reduce the persistence time and that varying the structure of the habitat can affect the dynamics of predator prey interactions. Moreover, we have shown that differences in the structure of the population regulatory processes may affect the persistence time of spatially explicit ecological interactions. However, habitat shape had no demonstrable effect on persistence in the experimental or stochastic simulation studies. Although, theoretically, habitat shape is predicted to affect species coexistence and persistence (Adler & Neurnberger 1994; Frank & Wissel 1998), here we have shown that the dynamical effect of the natural enemy significantly outweighs any effects that different spatial structures might have on increasing persistence time. While we show that habitat heterogeneity does not affect persistence, it clearly has an effect on the dynamical interaction between predators and prey. This led us to investigate the effects of differing dynamical regulatory processes explicitly in a broad range of spatial configurations. Taken with our findings, that density-dependent and independent processes, as described by autoregressive (AR) or moving average (MA) stochastic processes, respectively, are key determinants of interaction persistence time, it is clear that both patch dynamics and habitat spatial arrangement determine the metapopulation dynamics of predator prey interactions. The role of broad-scale patch heterogeneities and its effect on density dependence are known to affect metapopulation dynamics in resource consumer interactions. For example, Keitt & Johnson (1995) show, theoretically, that differences in global density dependence operating in predator prey metapopulations have a predominant effect on the regional dynamics. Localized patterns in the interaction between the predator and prey affect the time-scale over which these regulatory processes operate and consequently define the observed spatial pattern (rather than the persistence time of the interaction). It is predicted that the region-wide patterns of extinction and connectivity influence the density-dependent processes of prey regulation and predator foraging (Childs, Bonsall & Rees 004). Although it has been argued that metapopulation persistence and extinction are affected strongly by the rate at which the landscape changes (Adler & Neurnberger 1994; Keymer et al. 000; Childs et al. 004), the degree to which changes in patch connectivity affect persistence still remain a challenge for theoretical spatial ecology. In some ways, our metapopulation microcosms might be expected to behave as predicted by simple ecological theory. For example, the P* rule predicts that the prey species which supports the highest predator population (in the absence of the other species) will be the superior apparent competitor (Holt, Grover & Tilman 1994). Averaged across all habitat shapes, C. maculatus supports the higher parasitoid density in the pairwise host parasitoid interactions. However, among all the spatially structured habitats, Callosobruchus maculatus has the lower density in the pairwise host parasitoid metapopulations and yet is the species that dominates

8 906 J. C. Bull et al. Fig. 6. Box whisker plots showing the distribution, skew and kurtosis of simulated metapopulation persistence times across the full range of nine habitat configurations detailed in Fig. 1 under differing population regulatory treatments: AR(1), first-order autoregressive; AR(), second-order autoregressive; and AR()MA(1), second-order autoregressive first-order moving average. in apparent competition. The consequences of coupling patches, dispersal and extinction introduces additional complexities on the outcome of indirect ecological interactions that are not necessarily predicted by simple equilibrium-based effects such as the P* rule. Understanding how predation at the per patch level scales in a non-intuitive way to affect extinction and persistence at the regional-level requires further theoretical and empirical attention. Notwithstanding, apparent competition is known to have a predominant effect on the structure, dynamics and persistence of multispecies resource consumer interactions (Bonsall & Hassell 1997, 1998, 000; Chaneton & Bonsall 000). While it has been shown elsewhere that space can promote the persistence of this indirect interaction (Bonsall & Hassell 000; Bonsall et al. 005), the presence of a shared natural enemy can have an overwhelming effect on the regional metapopulation dynamics. Here, in the presence of the natural enemy (A. calandrae) and independent of habitat shape we show that the presence of C. maculatus decreases the observed persistence time of C. chinensis. On average, C. chinensis is lost a generation ( 4 weeks) earlier in the presence of the apparent competitor than in its absence. While the metapopulation processes of asynchrony in the local dynamics and rescue of extinction patches are operating in these different metapopulation structures, this process is highly variable over time and linked critically to the demographic processes operating at the local scale. Given that we identify no discernable difference in extinction risk, asynchrony and recolonization between habitat shapes, we postulate that local demographic stochastic factors predominately determine the likelihood and strength of these processes. Local stochastic processes are known to be important in determining ecological pattern (Moloney, Morin & Levin 1991), persistence (Frank 005) and dynamics (Bonsall & Hastings 004) in metapopulations. Given this, it is appropriate to consider whether the use of patch-scale determinants of connectivity is sufficient to predict the regional, metapopulation or landscape properties. While properties of metapopulation connectivity can depend on habitat structure, the size of the patches and species-specific traits (Tischendorf & Fahrig 000), the spatial configuration of patches can also affect the spatial dynamics, spread and characteristics of the ecological interaction (With & King 1999; Söndgerath & Schröder 00). For instance, Anderson & Danielson (1997) show, using a simulation model, that the number of corridor connections has no influence on the size of a metapopulation in a landscape unless there is an accompanying change in the uniformity of the distribution of corridor connections among patches. This has implications for correlates of metapopulation size such as the patterns of regulation and persistence. Here, we have shown that habitat configuration affects the dynamics of pairwise predator prey interactions while in more complex multispecies interactions, the structure of the metapopulation is relatively unimportant. Similarly, examples from studies on food-webs and experimental metacommunities (Forbes & Chase 00; Chase & Ryberg 004) further highlight the complexity that spatial scale introduces to understanding the local and regional aspects of species interactions. Spatial configurations of habitat patch networks affect the demographic processes of local interacting populations, the dynamics of dispersal and, consequently, the regional metapopulation processes of extinction, recolonizaton and persistence. Recognizing that different ecological processes operate at different spatial scales and under different patch configuration has important implications for the development of predictive landscape and metapopulation statistics (Mangel & Tier 1993; Hanski & Ovaskainen 000; Goodwin & Fahrig 00; Frank 005). In summary, we have shown that landscape-level factors such as the changes in patch availability and connectivity may not always lead to expected changes in persistence. The (spatial) lags introduced by changes in habitat structure must be sufficient to outweigh any destabilizing effects of the ecological interaction, in order to affect species persistence and coexistence. We emphasize the need for relevant ecological theory to be validated with appropriately designed replication ecological experiments. This approach and our findings have broader implications for the management of fragmented habitats, species interactions and conservation. Acknowledgements The work was supported by the NERC and the Royal Society. M.B.B. is a Royal Society University Research Fellow.

9 907 Multispecies metapopulation dynamics References Adler, F.R. & Neurnberger, B. (1994) Persistence in patchy irregular landscapes. Theoretical Population Biology, 45, Amarasekare, P. (004) Spatial variation and density-dependent dispersal in competitive coexistence. Proceedings of the Royal Society of London B, 71, Anderson, G.S. & Danielson, B.J. (1997) The effects of landscape composition and physiognomy on metapopulation size: the role of corridors. Landscape Ecology, 1, Bonsall, M.B., Bull, J.C., Pickup, N.J. & Hassell, M.P. (005) Indirect effects and spatial scaling affect the persistence of multispecies metapopulations. Proceedings of the Royal Society of London B, 7, Bonsall, M.B., French, D.R. & Hassell, M.P. (00) Metapopulation structures affect persistence of predator prey interactions. Ecology, 71, Bonsall, M.B. & Hassell, M.P. (1997) Apparent competition structures ecological assemblages. Nature, 388, Bonsall, M.B. & Hassell, M.P. (1998) The population dynamics of apparent competition in a host parasitoid assemblage. Ecology, 67, Bonsall, M.B. & Hassell, M.P. (000) The effects of metapopulation structure on indirect interactions in host parasitoids assemblages. Proceedings of the Royal Society of London B, 67, Bonsall, M.B. & Hastings, A. (004) Demographic and environmental stochasticity in predator prey metapopulation dynamics. Ecology, 73, Chaneton, E.J. & Bonsall, M.B. (000) Enemy-mediated apparent competition: empirical patterns and the evidence. Oikos, 88, Chase, J.M. & Ryberg, W.A. (004) Connectivity, scaledependence, and the productivity diversity relationship. Ecology Letters, 7, Childs, D.Z., Bonsall, M.B. & Rees, M. (004) Periodic local disturbance in host parasitoid metapopulations: host suppression and parasitoid persistence. Journal of Theoretical Biology, 7, Cox, D.R. & Oakes, D. (1984) Analysis of Survival Data. Chapman & Hall, London. Ellner, S.P., McCauley, E., Kendall, B.E., Briggs, C.J., Hosseini, P.R., Wood, S.N., Janssen, A., Sabelis, M.W., Turchin, P., Nisbet, R.M. & Murdoch, W.W. (001) Habitat structure and population persistence in an experimental community. Nature, 41, Etienne, R.S. & Heesterbeek, J.A.P. (000) On optimal size and number of reserves for metapopulation persistence. Journal of Theoretical Biology, 03, Forbes, A.E. & Chase, J.M. (00) The role of habitat connectivity and landscape geometry in experimental zooplankton metacommunities. Oikos, 96, Frank, K. (005) Metapopulation persistence in heterogeneous landscapes: lessons about the effect of stochasticity. American Naturalist, 165, Frank, K. & Wissel, C. (1998) Spatial aspects of metapopulation survival from model results to rules of thumb for landscape management. Landscape Ecology, 13, Goodwin, B.J. & Fahrig, L. (00) How does landscape structure affect landscape connectivity? Oikos, 99, Hagenaars, T.J., Donnelly, C.A. & Ferguson, N.M. (004) Spatial heterogeneity and the persistence of infectious diseases. Journal of Theoretical Biology, 9, Hanski, I. (1991) Single-species metapopulation dynamics concepts, models and observations. Biological Journal of the Linnean Society, 4, Hanski, I. (1999) Metapopulation Ecology. Oxford University Press, Oxford. Hanski, I.A. & Gaggiotti, O.E. (004) Ecology, Genetics and Evolution of Metapopulations. Academic Press, London. Hanski, I. & Ovaskainen, O. (000) The metapopulation capacity of a fragmented landscape. Nature, 404, Holt, R.D., Grover, J. & Tilman, D. (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. American Naturalist, 144, Holyoak, M. (000) Habitat patch arrangement and metapopulation persistence of predators and prey. American Naturalist, 156, Holyoak, M. & Lawler, S.P. (1996) Persistence of an extinctionprone predator prey interaction through metapopulation dynamics. Ecology, 77, Huffaker, C.B., Shea, K.P. & Herman, S.G. (1963) Experimental studies on predation: complex dispersion and levels of food in an acarine predator prey interaction. Hilgardia, 34, Jonzén, N., Wilcox, C. & Possingham, H.P. (004) Habitat selection and population regulation in temporally fluctuating environments. American Naturalist, 164, E103 E114. Keitt, T.H. & Johnson, A.R. (1995) Spatial heterogeneity and anomalous kinetics emergent patterns in diffusionlimited predator prey interactions. Journal of Theoretical Biology, 17, Keymer, J.E., Marquet, P.A., Velasco-Hernandez, J.X. & Levin, S.A. (000) Extinction thresholds and metapopulation persistence in dynamic landscapes. American Naturalist, 156, Legendre, P. & Legendre, L. (1998) Numerical Ecology. Elsevier, Amsterdam. Levins, R. (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bulletin of Entomological Research, 15, Mangel, M. & Tier, C. (1993) A simple direct method for finding persistence times of populations and application to conservation problems. Proceedings of the National Academy of Sciences USA, 90, Moloney, K.A., Morin, A. & Levin, S.A. (1991) Interpreting ecological patterns generated through simple stochastic processes. Landscape Ecology, 5, Nicholson, A.J. & Bailey, V.A. (1935) The balance of animal populations. Part I. Proceedings of the Zoological Society of London, 3, Pimentel, D., Nagel, W.P. & Madden, J.L. (1963) Space time structure and the survival of parasite host systems. American Naturalist, 97, Royama, T. (199) Analytical Population Dynamics. Chapman & Hall, London. Snyder, R.E. & Chesson, P. (003) Local dispersal can facilitate coexistence in the presence of permanent spatial heterogeneity. Ecology Letters, 6, Söndgerath, D. & Schröder, B. (00) Population dynamics and habitat connectivity affecting the spatial spread of populations a simulation study. Landscape Ecology, 17, Tischendorf, L. & Fahrig, L. (000) How should we measure landscape connectivity? Landscape Ecology, 15, With, K.A. & King, A.W. (1999) Extinction thresholds for species in fractal landscapes. Conservation Biology, 31, Wright, S. (1940) Breeding structure of populations in relation to speciation. American Naturalist, 74, Received 6 October 005; accepted 6 March 006