Journal of Animal Ecology

2006

75

,

899–907

© 2006 The Authors.Journal compilation© 2006 British Ecological Society

Blackwell Publishing Ltd

Habitat shape, metapopulation processes and the dynamics 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 per-sistence and extinction are explored in a multispecies resource–consumer interaction.

2.

The spatial dynamics of the indirect interaction between two prey species (

Calloso-bruchus chinensis

,

Callosobruchus maculatus

) and a predator (

Anisopteromalus calandrae

)are investigated and we show how the persistence time of this interaction is altered indifferent habitat configurations by the presence of an apparent competitor.

3.

Habitat structure has differential effects on the dynamics of the resource–consumerinteraction. 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 expectationsfrom theory, habitat shape has no significant effect on persistence time of the full, three-species resource–consumer assemblage.

4.

A stochastic metapopulation model for a range of habitat configurations, incor-porating different forms of regulatory processes, highlights that it is the spatially explicitpopulation dynamics rather than the shape of the metapopulation that is the principaldeterminant of interaction persistence time.

Keywords

:

Anisopteromalus

, apparent competition,

Callosobruchus

, extinction, host–parasitoid interaction, population dynamics, time-series, regulatory process, spatialarrangement

Journal of Animal Ecology

(2006)

75

, 899–907doi: 10.1111/j.1365-2656.2006.01107.x

Introduction

Spatial heterogeneity and habitat structure has wide-ranging ecological implications, from the persistence ofinfectious diseases (Hagenaars, Donnelly & Ferguson2004) through to the design of nature reserves (Etienne& Heesterbeek 2000). Both theoretical and empiricalstudies of spatial structure have progressed from simplyproposing that spatial mechanisms might increase thepersistence of ecological systems (Nicholson & Bailey1935; Wright 1940; Huffaker, Shea & Herman 1963;Pimentel, Nagel & Madden 1963) to quantitative inves-tigations of the effects of metapopulation structure onsingle species (Levins 1969; Hanski 1991; Hanski 1999),

pairwise interactions (Holyoak & Lawler 1996; Ellner

et al

. 2001; Bonsall, French & Hassell 2002) and mul-tispecies assemblages (Forbes & Chase 2002; Chase &Ryberg 2004; Bonsall

et al

. 2005). Although it is nowrelatively well established that metapopulation struc-ture has important implications for the dynamics andpersistence for a range of ecological scenarios (Hanski& Gaggiotti 2004), a remaining challenge is to explorethe effects of habitat connectivity, patch arrangementsand patch dynamics on the metapopulation processesof persistence and extinction. While there is a consid-erable body of theoretical work suggesting that habitatshape and spatial heterogeneity is of importance indetermining the outcome of resource–consumer inter-actions (Holyoak 2000; Snyder & Chesson 2003; Amar-asekare 2004; Jonzén, Wilcox & Possingham 2004), theeffects of regional spatial heterogeneity on the persist-ence of more complex ecological interactions are oftenunclear (Hagenaars

et al

. 2004). In particular, how

Correspondence: Dr Mike Bonsall, Department of Zoology,University of Oxford, South Parks Road, Oxford, Oxon. OX13PS, UK. Tel: 01865 281064; Fax: 01865 310447. E-mail:michael.bonsall@zoo.ox.ac.uk

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spatially variable habitats affect local and regionalecological processes such as predator–prey interactions,resource–consumer dynamics and indirect speciesinteractions remains largely unexplored.

Previously, using predator–prey metapopulations, ithas been shown that large scale spatial structure can affectthe persistence of these extinction-prone resource–consumer interactions (Holyoak & Lawler 1996; Ellner

et al

. 2001; Bonsall, French & Hassell 2002; Bonsall &Hastings 2004). More recently, this effect has beenextended to show how metapopulation structures andspatial scale can influence the outcome of more com-plex multispecies interactions (Bonsall

et al

. 2005). Byexploring the effects of apparent competition (wheretwo species that do not compete for resource, share a com-mon natural enemy), it has been illustrated that spatialstructure can mitigate the ecological effects of this indi-rect interaction. Four conditions for metapopulationpersistence (e.g. Hanski 1999) have been shown to under-pin these multispecies interactions. First, single patchesare capable of supporting host populations in the absenceof parasitoids. Secondly, patches are at high risk of extinc-tion in the presence of parasitoids. Thirdly, there is asyn-chrony across space and through time between patches,and finally there is rescue of extinct patches (Bonsall

et al

.2005).

Here, we extend this theme to explore how habitat shapeinfluences the persistence and dynamics of resource–consumer metapopulations. Using replicated laboratorymicrocosms we investigate the effects of parasitism(pairwise resource–consumer interactions) andshared parasitism (apparent competitive interactions)over a wide range of habitat designs. Metapopulationshapes are varied in the degree of connectivity (number

of links between patches vary but total number of patchesis constant). We illustrate that the effects of apparentcompetition on the persistence time of the multispeciesinteraction are observed over the full range of habitatdesigns. Moreover, while habitat shape affects thepopulation dynamics and regulatory processes of theresource–consumer interaction, contrary to expectationthe shape of the habitat has no effect on the persistencetime of either the pairwise or apparent competitive assem-blages. Having demonstrated the importance of habitatshape on population dynamical processes, we furtherexplore metapopulation persistence and habitat shapethrough the development of a number of stochasticpopulation models incorporating differing regulatoryprocesses and embedding these within an expandedrange of patch configurations. These hypotheticalhabitat designs vary in more than just the variance ofconnectivity, with both the mean number of connectionsand the maximum distance across the metapopulationbeing explored. Across all habitat shapes tested, wefind that it is the population regulatory processes,not the spatial arrangement of patches which affectspersistence time.

Materials and methods

Laboratory microcosms were used to explore the hypo-thesis that habitat shape affects the persistence of anapparent competition interaction between the bruchidbeetles,

Callosobruchus maculatus

(Fabricius) (Coleop-tera: Bruchidae) and

C. chinensis

(L.) (Coleoptera: Bruch-idae), mediated through parasitism by the parasitoid,

Anisopteromalus calandrae

(Howard) (Hymenoptera:Pteromalidae).

Clear, plastic boxes (73

×

73

×

30 mm) were used as thebaseline ‘patch’ for the study. Patches had a hole (4·4 mmdiameter) placed in each of their four sides which couldeither be blocked or lengths (50 mm) of plastic tubeinserted to connect patches horizontally into latticearrangements of various designs. A single-layer lattice ofthese patches was used for treatments that includedonly one bruchid species. In the treatments includingboth bruchids, patches were stacked into double-layersystems. In these cases, top- and bottom-layer patcheswere connected by a 25 mm-diameter mesh-covered hole.The mesh (hole size: 2 mm) prevented vertical movementby bruchids and, consequently, any direct, interspecificresource competition. However, this tested experi-mental design did not inhibit the foraging activity of theparasitoid over both bruchid species and allowed anapparent competitive interaction to be established.

Four different experimental arrangements of ninepatches were assembled (Fig. 1a–d) in which the meanconnectivity was constant (mean connections per patch =1·78) but the variance in connectivity differed [varianceof connectivity: ‘line’ (treatment 1) = 0·194, ‘I-design’(treatment 2) = 0·694, ‘cross’ (treatment 3) = 0·944 and

Fig. 1. Schematic diagram showing the nine spatial arrangements of patches used.Designs a–d alone were constructed as laboratory experimental treatments, while allconfigurations were included in the stochastic process models. See Table 1 for details ofmean and variance in connectivity between patches.

901

Multispecies metapopulation dynamics

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‘double-star’ (treatment 4) = 1·694]. Three differentspecies combinations were established in each of thehabitat designs:

C. maculatus

with

A. calandrae

and

C.chinensis

with

A. calandrae

as separate, two-speciesinteractions and the full, three-species, apparentcompetition 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 bruchidsinto every patch each week. In the cases of double-layerlattices, two replicates of each treatment were seeded withfour pairs of

C. maculatus

on the upper lattice and fourpairs of

C. chinensis

on the lower lattice, and two replicatesthe other way around. On the fourth week, a further threebeans were placed in each patch (three on each level ofdouble-layer patches) and new bruchids emerged fromthe beans introduced in week 1. Subsequently, beanresources were replaced following a 4-week resourcerenewal scheme, with the oldest three beans being replacedfrom each patch every week. Removed beans were storedfor a further 4 weeks and any newly emerging animalswere released back into the appropriate patch.

After the host species had become established forseveral generations without dispersal between patches,dispersal for 2 h each week was initiated. This length ofdispersal window has been shown previously to resultin a significant increase in interaction persistence timecompared to unlimited dispersal (Bonsall

et al

. 2005).Parasitoids were introduced after a further two hostgenerations. Four pairs of wasps were introduced over2 consecutive weeks into three different patches in themetapopulations. Time-series for all species were obtainedby counting both alive and dead insects each week fromevery patch (dead insects were then removed). All experi-ments were undertaken in controlled environmentalconditions (30

°

C, 70% relative humidity, 16 : 8 light :dark cycle).

Asynchrony in the dynamics between patches wasinvestigated through spatiotemporal semivariogramsfor each metapopulation (of

n

patches), which were cal-culated using where

x

is the individual species, patch specific growth rate forequally weighted time-point

τ

and spatial referencepoint (Legendre & Legendre 1998). This statistic cate-gorizes the squared differences in population growthrate between all possible pairs of patches into groupsaccording to the minimum number of steps (

d

) betweenthe

i

th and

j

th patch in the metapopulation. Means,

γ

(

d

,

τ

), for each of these distance categories representthe level of asynchrony and are presented for each dis-tance (

d

) and time-point (

τ

).The potential for extinct patches to be recolonized

was determined by calculating the conditional prob-ability that a patch, in which a given species was absentat time

τ

, was subsequently recolonized. Adults had to be

absent from any given patch for 4 weeks continuouslyin the case of hosts or 2 weeks continuously in the caseof parasitoids, in order to allow for any developing insectsto emerge as adults. This ensured that immigration fromneighbouring patches was the only possible source ofinsects present in patches from which they were foundto be extinct.

To test the hypothesis that habitat structure affects thedynamics of the predator–prey assemblage we explore,using analysis of covariance (with population densityas a continuous variable and habitat shape as a categoricalvariable), how the regulatory processes operating in thepersistent, pairwise, host–parasitoid (

C. maculatus–A.calandrae

) interaction differ between habitat types.We use conventional population ecological analysis of re-gressing net reproductive rate [ ln(

N

t

+1

/

N

t

)] on laggedpopulation density (Royama 1992) and include habitatshape as a covariate.

Metapopulation persistence times for the pairwise(

C. chinensis–A. calandrae

) and apparent competitive(

C. chinensis

–

C. maculatus

–

A. calandrae

) interactionswere compared using survival analyses (Cox & Oakes1984) and any replicates persisting at the end of the ex-periment were censored. Model simplification (stepwiseelimination of non-significant explanatory variables)was used to determine the most appropriate, minimaladequate model (the model retaining only significantterms) with residual errors for this survival regressiondescribed appropriately by a Weibull distribution.

Further investigation of the relationship between dynam-ical processes and habitat shape were conducted throughdevelopment and analysis of population simulationmodels applied to an expanded range of patch config-urations (Fig. 1a–i). Patch-specific, population dynamicswere modelled by using stochastic population models.In particular, autoregressive processes were used todescribe time-lagged density-dependent processes (e.g.

N

i

,

t

,

N

i

,

t

−

1

) while moving average processes were used todescribe density-independent processes (e.g.

Z

i

,

t

). Forinstance, dynamical changes in the

i

th patch driven bya second-order density-dependent process [AR(2)] anda first-order moving average process [MA(1)] aredescribed by (Bonsall

et al

. 2002):

where

f

(·) is the underlying stochastic process and

ε

t

is a independent, identically distributed randomvariable. Three different population dynamic scenariosoperating at the patch-level were considered: a first-orderdensity-dependent process [AR(1)], a second-orderdensity-dependent process [AR(2)] and a second-order density-dependent process coupled to a first-order

γ τ τ τ( , ) / ( )d x xin

yn

i j= ∑ ∑ −= =1 2 1 12

N f N N Zi t i t i t i t t, , , , ( , , , )+ −=1 1 ε

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density-independent process [AR(2)MA(1)]. Net changesin abundance within the

i

th patch are also influencedthrough dispersal:

where

δ

i

is the density-independent dispersal fractionfrom the

i

th patch,

N

i

and

N

j

are the numbers of animalsin the

i

th and

j

th patch and

λ

ij

is the connectivity matrixthat determines the possible links between patches(and allows the effects of different habitat shapes to beexplored). In the analysis, habitat shape and regulatoryform were considered as separate, categorical variablesexplaining variance in persistence time. All analyseswere completed in

-

.

In Fig. 2, we show representative time-series from eachof the (replicated) pairwise interactions (

C. chinensis–A. calandrae

,

C. maculatus–A. calandrae

) and the appar-ent competitive interaction (

C. chinensis–C. maculatus–A. calandrae

) from the different habitat shapes. Acrossall habitat types, all replicates of

C. maculatus–A. calandrae

persisted over the course of the experiment (

∼

32 weeks).We use these time-series to explore how habitat shapeaffects (meta)population dynamics of the resource–consumer interaction. In the apparent competitive

interaction,

C. chinensis

is always the species that isdriven to extinction (Fig. 2i–l). To explore the hypo-thesis that habitat type and assemblage complexityaffect persistence and metapopulation processes wemake comparisons between this pairwise interaction(

C. chinensis–A. calandrae

) and the full three-speciesapparent competitive interaction.

Testing the hypothesis that asynchrony is affected byspatial and temporal processes reveals that correlationsin patch-specific population growth rates are highlyvariable across space and through time. Temporallyexplicit variograms of the full three-species interactionand the pairwise

C. chinensis–A. calandrae

metapopu-lations illustrate that asynchrony increases with dis-tance between patches and varies widely over time(Fig. 3). The highly variable nature of the asynchronyover time masks any clear differences between treat-ments. However, the parasitoid appears to be more inphase among patches in the two species

C. chinensis–A. calandrae

interaction than in the apparent competitionassemblage (Fig. 3).

To determine the recolonization potential and re-scue of extinct patches, conditional probabilities werecalculated for the re-invasion of each of the species inthe apparent competitive interaction (Table 1). While

N N Ni t i i ijj

p

j, ( ) +=

= − + ∑δ δ λ11

Fig. 2. 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 themetapopulation while C. chinensis is the species that is always driven extinct in the apparent competitive interaction − see text forfurther details (solid grey line: C. maculatus; solid black line: C. chinensis; dashed black line: A. calandrae).

903Multispecies metapopulation dynamics

© 2006 The Authors.Journal compilation© 2006 British Ecological Society, Journal of Animal Ecology, 75, 899–907

all three species in the study show the potential forrecolonization, the rate of recolonization variesbetween species and amongst habitat arrangement(Table 1). Parasitoids demonstrate the greatest frequencyof recolonization, followed by C. maculatus, which wasthe superior apparent competitor in all cases. Re-colonization by C. chinensis into patches where it wasextinct was rare and in some cases did not occur at all.

The average abundance (with standard errors), acrossall habitat shapes, of C. chinensis in the presence of the wasp(A. calandrae) was 81·18 (5·33) and the abundance of theparasitoid was 25·69 (0·91). In comparison, the abundanceof C. maculatus was 60·98 (2·15) and the abundance of A.calandrae was 38·29 (2·18). The C. chinensis–A. calandraeinteraction was extinction prone and persists for only

about 17 weeks (mean persistence time 17·20 (2·11)weeks). In contrast, the dynamics of the C. maculatus–A. calandrae interactions showed sustained long-termfluctuations across all habitat shapes (Fig. 1a–d). Dif-ferences in temporal density-dependence occur in thisresource–consumer interaction among the differenthabitats (Fig. 4): regression of the net reproductive ratevs. lagged population density shows that the dynamicsof C. maculatus (in the presence of A. calandrae) aredescribed by different density-dependent relationships(Fig. 4). In particular, model simplification reveals thatthe dynamics in the two habitats with low variance inconnectivity (‘line’ and ‘I-design’) are described by thesame density-dependent relationship, whereas separaterelationships are required for each of the two otherhabitats (with higher variance in connectivity, ‘cross’ and‘double-star’) (population size–habitat shape interactionF2,499 = 3·126, P = 0·0447).

Fig. 3. Semi-variograms of asynchrony in patch-specific growth rate. Representative replicates are shown for all four habitat shapes, top row of foursemivariograms 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 ofasynchrony were made using – see text for further details.γ τ τ τ( , ) / ( )d x xi

njn

i j= ∑ ∑ −= =1 2 1 12

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Overall, in the nine-patch metapopulations, the pres-ence of an apparent competitor (C. maculatus) affectedthe persistence of the multispecies assemblage (three-species persistence time: mean = 13·63 (SE = 1·46) weeks;two-species persistence time: mean = 17·20 (SE = 2·11)weeks). The distribution, skew and kurtosis for persist-ence times for the pairwise and apparent competitiveinteractions in the different habitats are shown in Fig. 5.Mean (SE) persistence times (in weeks) for the pairwise(C. chinensis–A. calandrae) interaction were 16·25 (1·7),17·25 (4·99), 20·33 (5·89) and 15·75 (5·43) for each of thehabitat types (see Fig. 1a–d for patch arrangements).Similarly, persistence times for the apparent competi-tive interaction were 14·75 (3·59), 10·5 (1·04), 16·25 (4·17)and 13·0 (2·27) for each of the habitat types (Fig. 1a–d).Model simplification revealed that the only significantdeterminant on persistence time was the presence of theapparent competitor (C. maculatus). Across all habitattreatments, there was a statistically significant decreasein metapopulation persistence time due to presence of

the apparent competitor ( = 4·048, P = 0·0424). Despitealmost an order of magnitude range in the variance ofconnectivity between the habitat shapes and differencesin the metapopulation processes (asynchrony and rec-olonization in individual patches) operating in thesedifferent habitats, there was no significant difference inpersistence time of the pairwise and apparent competitivepredator–prey assemblage between spatial arrangements( = 0·0049, P = 0·994). There was also no significantinteraction effect between assemblage type (pairwise,apparent competitive) and habitat shape on meta-population persistence time ( = 3·766, P = 0·152).

Stochastic process models incorporating differentforms of temporal autocorrelation were used to invest-igate further the relationship between habitat shapeand population regulatory processes. Across all patcharrangements, habitat shape had no significant impacton persistence time (F8,1323 = 0·728, P = 0·666). How-ever, regulatory process did have a significant effect onpersistence time (F2,1323 = 121·756, P < 0·001) (Fig. 6).

Table 1. Connectivity and species-specific patch recolonization potentials for three species, apparent competition assemblages innine spatial arrangements of nine-patch habitats

Habitat shape treatments

ConnectivityMaximum stepsacross habitat

Recolonization probability

Mean Variance C. chinensis C. maculatus A. calandrae

1 (‘line’) 1·78 0·194 8 0·01 0·20 0·172 (‘I-design’) 1·78 0·694 6 0·01 0·18 0·183 (‘cross’) 1·78 0·944 4 0·00 0·06 0·534 (‘double-star’) 1·78 1·694 4 0·00 0·11 0·335 (‘long cross’) 1·78 0·944 6 Simulated populations6 (‘open Union Jack’) 1·78 5·44 2 Simulated populations7 (‘ring’) 2·00 0·00 4 Simulated populations8 (‘square’) 2·67 0·50 4 Simulated populations9 (‘closed Union Jack’) 3·56 2·78 2 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) inthe 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).

χ12

χ12

χ22

905Multispecies metapopulation dynamics

© 2006 The Authors.Journal compilation© 2006 British Ecological Society, Journal of Animal Ecology, 75, 899–907

Under AR(1) processes, the mean persistence time(12·98) of the metapopulation systems was signifi-cantly longer than persistence under an AR(2) or anAR(2)MA(1) process (5·74, 5·29, respectively).

Discussion

Here we have evaluated the metapopulation processesin a multispecies host–parasitoid assemblage. We haveshown that the presence of an apparent competitor can

reduce the persistence time and that varying the struc-ture of the habitat can affect the dynamics of predator–prey interactions. Moreover, we have shown thatdifferences in the structure of the population regulatoryprocesses may affect the persistence time of spatiallyexplicit ecological interactions. However, habitat shapehad no demonstrable effect on persistence in the ex-perimental or stochastic simulation studies. Although,theoretically, habitat shape is predicted to affect speciescoexistence and persistence (Adler & Neurnberger1994; Frank & Wissel 1998), here we have shown thatthe dynamical effect of the natural enemy significantlyoutweighs any effects that different spatial structuresmight have on increasing persistence time.

While we show that habitat heterogeneity does notaffect persistence, it clearly has an effect on the dynamicalinteraction between predators and prey. This led us toinvestigate the effects of differing dynamical regulatoryprocesses explicitly in a broad range of spatial configura-tions. Taken with our findings, that density-dependentand independent processes, as described by autoregressive(AR) or moving average (MA) stochastic processes,respectively, are key determinants of interaction per-sistence time, it is clear that both patch dynamics andhabitat spatial arrangement determine the metapopu-lation dynamics of predator–prey interactions. The roleof broad-scale patch heterogeneities and its effect ondensity dependence are known to affect metapopula-tion dynamics in resource–consumer interactions. Forexample, Keitt & Johnson (1995) show, theoretically,that differences in global density dependence operatingin predator–prey metapopulations have a predominanteffect on the regional dynamics. Localized patterns inthe interaction between the predator and prey affect thetime-scale over which these regulatory processes oper-ate and consequently define the observed spatial pattern(rather than the persistence time of the interaction). It ispredicted that the region-wide patterns of extinctionand connectivity influence the density-dependent pro-cesses of prey regulation and predator foraging (Childs,Bonsall & Rees 2004). Although it has been argued thatmetapopulation persistence and extinction are affectedstrongly by the rate at which the landscape changes(Adler & Neurnberger 1994; Keymer et al. 2000; Childset al. 2004), the degree to which changes in patch con-nectivity affect persistence still remain a challenge fortheoretical spatial ecology.

In some ways, our metapopulation microcosms mightbe expected to behave as predicted by simple ecologicaltheory. For example, the P* rule predicts that the preyspecies which supports the highest predator popula-tion (in the absence of the other species) will be thesuperior apparent competitor (Holt, Grover & Tilman1994). Averaged across all habitat shapes, C. maculatussupports the higher parasitoid density in the pairwisehost–parasitoid interactions. However, among all thespatially structured habitats, Callosobruchus maculatushas the lower density in the pairwise host–parasitoidmetapopulations and yet is the species that dominates

Fig. 5. Box–whisker plots showing the distribution, skew andkurtosis of metapopulation persistence times for (a) the pairwiseinteraction between C. chinensis and A. calandrae and (b) theapparent competitive interaction. The central line in each boxshows the median time to extinction (in weeks), with the boxextending to cover the interquartile range and whiskersextending to 1·5 times the interquartile range (habitat treat-ment codes are 1 = ‘line’, 2 = ‘I-design’, 3 = ‘cross’ and 4 =‘double-star’).

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in apparent competition. The consequences of couplingpatches, dispersal and extinction introduces additionalcomplexities on the outcome of indirect ecological inter-actions that are not necessarily predicted by simpleequilibrium-based effects such as the P* rule. Under-standing how predation at the per patch level scales ina non-intuitive way to affect extinction and persistenceat the regional-level requires further theoretical andempirical attention.

Notwithstanding, apparent competition is known tohave a predominant effect on the structure, dynamicsand persistence of multispecies resource–consumer inter-actions (Bonsall & Hassell 1997, 1998, 2000; Chaneton& Bonsall 2000). While it has been shown elsewherethat space can promote the persistence of this indirectinteraction (Bonsall & Hassell 2000; Bonsall et al. 2005),the presence of a shared natural enemy can have anoverwhelming effect on the regional metapopulationdynamics. Here, in the presence of the natural enemy(A. calandrae) and independent of habitat shape weshow that the presence of C. maculatus decreases theobserved persistence time of C. chinensis. On average,C. chinensis is lost a generation (∼4 weeks) earlier in thepresence of the apparent competitor than in its absence.While the metapopulation processes of asynchrony inthe local dynamics and rescue of extinction patches areoperating in these different metapopulation structures,this process is highly variable over time and linked crit-ically to the demographic processes operating at the localscale. Given that we identify no discernable differencein extinction risk, asynchrony and recolonizationbetween habitat shapes, we postulate that local demo-graphic stochastic factors predominately determinethe likelihood and strength of these processes. Localstochastic processes are known to be important indetermining ecological pattern (Moloney, Morin &

Levin 1991), persistence (Frank 2005) and dynamics(Bonsall & Hastings 2004) in metapopulations.

Given this, it is appropriate to consider whether theuse of patch-scale determinants of connectivity is suf-ficient to predict the regional, metapopulation or land-scape properties. While properties of metapopulationconnectivity can depend on habitat structure, the sizeof the patches and species-specific traits (Tischendorf& Fahrig 2000), the spatial configuration of patchescan also affect the spatial dynamics, spread and char-acteristics of the ecological interaction (With & King1999; Söndgerath & Schröder 2002). For instance,Anderson & Danielson (1997) show, using a simulationmodel, that the number of corridor connections has noinfluence on the size of a metapopulation in a land-scape unless there is an accompanying change in theuniformity of the distribution of corridor connectionsamong patches. This has implications for correlates ofmetapopulation size such as the patterns of regulationand persistence. Here, we have shown that habitat con-figuration affects the dynamics of pairwise predator–prey interactions while in more complex multispeciesinteractions, the structure of the metapopulation is rel-atively unimportant. Similarly, examples from studieson food-webs and experimental metacommunities(Forbes & Chase 2002; Chase & Ryberg 2004) furtherhighlight the complexity that spatial scale introduces tounderstanding the local and regional aspects of speciesinteractions.

Spatial configurations of habitat patch networksaffect the demographic processes of local interactingpopulations, the dynamics of dispersal and, conse-quently, the regional metapopulation processes ofextinction, recolonizaton and persistence. Recognizingthat different ecological processes operate at differentspatial scales and under different patch configurationhas important implications for the development ofpredictive landscape and metapopulation statistics(Mangel & Tier 1993; Hanski & Ovaskainen 2000;Goodwin & Fahrig 2002; Frank 2005).

In summary, we have shown that landscape-levelfactors such as the changes in patch availability andconnectivity may not always lead to expected changesin persistence. The (spatial) lags introduced by changesin habitat structure must be sufficient to outweighany destabilizing effects of the ecological interaction,in order to affect species persistence and coexistence.We emphasize the need for relevant ecological theoryto be validated with appropriately designed replicationecological experiments. This approach and our find-ings have broader implications for the managementof fragmented habitats, species interactions andconservation.

Acknowledgements

The work was supported by the NERC and the RoyalSociety. M.B.B. is a Royal Society University ResearchFellow.

Fig. 6. Box–whisker plots showing the distribution, skew and kurtosis of simulatedmetapopulation persistence times across the full range of nine habitat configurationsdetailed in Fig. 1 under differing population regulatory treatments: AR(1), first-orderautoregressive; AR(2), second-order autoregressive; and AR(2)MA(1), second-orderautoregressive–first-order moving average.

907Multispecies metapopulation dynamics

© 2006 The Authors.Journal compilation© 2006 British Ecological Society, Journal of Animal Ecology, 75, 899–907

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Received 26 October 2005; accepted 6 March 2006