FIRE INCREASES INVASIVE SPREAD OF MOLINIA CAERULEA MAINLY THROUGH CHANGES IN DEMOGRAPHIC PARAMETERS

2097

Ecological Applications, 15(6), 2005, pp. 2097–2108q 2005 by the Ecological Society of America

FIRE INCREASES INVASIVE SPREAD OF MOLINIA CAERULEA MAINLYTHROUGH CHANGES IN DEMOGRAPHIC PARAMETERS

HANS JACQUEMYN,1,4 REIN BRYS,1,2 AND MICHAEL G. NEUBERT3

1Laboratory for Forest, Nature and Landscape Research, Catholic University of Leuven, Vital Decosterstraat 102,B-3000 Leuven, Belgium

2Institute of Nature Conservation, Kliniekstraat 25, B-1070 Brussels, Belgium3Biology Department, MS-34, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543-1049 USA

Abstract. We investigated the effects of fire on population growth rate and invasivespread of the perennial tussock grass Molinia caerulea. During the last decades, this specieshas invaded heathland communities in Western Europe, replacing typical heathland speciessuch as Calluna vulgaris and Erica tetralix. M. caerulea is considered a major threat toheathland conservation. In 1996, a large and unintended fire destroyed almost one-third ofthe Kalmthoutse Heide, a large heathland area in northern Belgium. To study the impactof this fire on the population dynamics and invasive spread of M. caerulea, permanentmonitoring plots were established both in burned and unburned heathland. The fate of eachM. caerulea individual in these plots was monitored over four years (1997–2000). Patternsof seed dispersal were inferred from a seed germination experiment using soil cores sampledone month after seed rain at different distances from seed-producing plants. Based on thesemeasures, we calculated projected rates of spread for M. caerulea in burned and unburnedheathland. Elasticity and sensitivity analyses were used to determine vital rates that con-tributed most to population growth rate, and invasion speed. Invasion speed was, on average,three times larger in burned compared to unburned plots. Dispersal distances on the otherhand, were not significantly different between burned and unburned plots indicating thatdifferences in invasive spread were mainly due to differences in demography. Elasticitiesfor fecundity and growth of seedlings and juveniles were higher for burned than for unburnedplots, whereas elasticities for survival were higher in unburned plots. Finally, a life tableresponse experiment (LTRE) analysis revealed that the effect of fire was mainly contributedby increases in sexual reproduction (seed production and germination) and growth of seed-lings and juveniles. Our results clearly showed increased invasive spread of M. caeruleaafter fire, and call for active management guidelines to prevent further encroachment ofthe species and to reduce the probability of large, accidental fires in the future. Mowingof resprouted plants before flowering is the obvious management tactic to halt massiveinvasive spread of the species after fire.

Key words: disturbance; elasticity; fire; integrodifference equations; invasive spread; LTRE;matrix population model; Molinia caerulea; sensitivity.

INTRODUCTION

European heathlands are generally known as lowproductivity ecosystems characterized by dominance oftypical dwarf shrub species such as Calluna vulgarisand Erica tetralix. Traditionally, these heathland sys-tems were maintained by small-scale land use practicessuch as sod cutting, grazing by sheep, or controlledburning in winter (Gimingham 1972). During the lastdecades, however, typical heathland species have beengradually replaced by more competitive species suchas Molinia caerulea and Deschampsia flexuosa. In par-ticular, the distribution and abundance of M. caeruleahas increased in Western Europe to such an extent thatM. caerulea has become the dominant species in many

Manuscript received 19 November 2004; revised 8 March2005; accepted 22 March 2005; Corresponding Editor: C. L.Boggs.

4 E-mail: [email protected]

heathland communities (e.g., Hansen 1976, Berendseet al. 1994, Chambers et al. 1999). Increased nitrogendeposition and changes in management have been pro-posed as the main causes for this shift in species com-position (Aerts and De Caluwe 1989, Aerts 1993, Ber-endse et al. 1994, Limpens et al. 2003, Tomassen et al.2003). As a result, M. caerulea encroachment is con-sidered a major threat to heathland conservation inWestern Europe (Marrs et al. 2004).

As M. caerulea is a deciduous grass species thatproduces large amounts of litter each year, this shiftfrom fields dominated by C. vulgaris to those domi-nated by M. caerulea has resulted in several large,mostly unintended fires, especially in dry heathlands.Fire may dramatically affect population dynamics ofplants (reviewed in Noble and Slatyer 1980). Indeed,for most species, population dynamics have beenshown to be very different in burned and unburned sites(e.g., Silva et al. 1991, Canales et al. 1994, Caswell

2098 HANS JACQUEMYN ET AL. Ecological ApplicationsVol. 15, No. 6

and Kaye 2001, Garnier and Dajoz 2001a, Kaye et al.2001, Satterthwaite et al. 2002, Quintana-Ascencio etal. 2003, Menges and Quintana-Ascencio 2004). Firehas been shown to increase population growth rates byincreasing seed production (McConnell and Menges2002), seed germination rates (Canales et al. 1994,Menges and Dolan 1998), or growth (Lamont andWiens 2003). Moreover, because of changes in seedproduction rates and vegetation structure, fire can alsobe expected to alter the mean seed dispersal distance(Nathan and Muller-Landau 2000) and hence the in-vasion speed of the species (Neubert and Caswell 2000,Caswell et al. 2003), although at present this has notyet been rigorously investigated.

To give a full account of the relative importance ofdispersal and demographic parameters in determininginvasive spread of species and how these are affectedby disturbances such as fire, one needs to incorporateboth parameters into one single measure. A measurethat integrates dispersal and population vital rates isthe invasion speed, c* (Neubert and Caswell 2000, Cas-well et al. 2003). Like population growth rate, l, in-vasion speed allows calculation of sensitivity and elas-ticity measures, which determine how invasion speedwould respond to changes in demographic and dispersalparameters, and life table response experiments(LTRE), which determine how differences in modelparameters between different populations contribute todifferences in their invasion speeds. Because prospec-tive perturbation analyses of c* identify the life cyclestages that are most important in determining popu-lation growth rate and invasive spread (see Caswell2000), they are very useful in resolving which stagesare crucial to attack when attempting to slow invasivespread (Fagan et al. 2002). Furthermore, methods tomodel the impact of temporally heterogeneous envi-ronments on invasion wave speed have been developed(Neubert et al. 2000). The latter allow calculating time-averaged invasion rates in periodic environments andexpected time-averaged invasion rates in stochastic en-vironments (Neubert et al. 2000, Neubert and Parker2004).

In this study, we examined how fire affected dis-persal, population dynamics, and invasion speed of theperennial tussock-forming grass M. caerulea in theKalmthoutse Heide, a relatively large heathland areain the northern part of Belgium. In April 1996, a largeand unintended fire burned almost one-third of the area.In 1997, burned M. caerulea plants had resprouted andproduced seeds. Detailed demographic data were col-lected for four years between 1997 and 2000, whereasseed dispersal distances were inferred from a seed ger-mination experiment using soil cores sampled onemonth after seed rain in 1997. More specifically, weinvestigated the following questions: (1) How does fireaffect population growth rate and invasion speed of M.caerulea in dry heathland? (2) Which vital rates aremost important in determining population growth rates

and which parameters (demographic or dispersal) aremost important in determining invasion speed? (3)What kind of management strategies can be deducedfrom the observed patterns of invasion?

METHODS

Study plant

Molinia caerulea (purple moor-grass) is a tall, pe-rennial grass species that occurs throughout much ofEurope and that extends its distribution to North Africa,Caucasus, and Siberia (Taylor et al. 2001). The speciesoccupies a wide range of habitats (ranging from foreststo grasslands to heathlands) and soil types (rangingfrom dry acid sands to wet calcareous bogs). In Bel-gium, the distribution of M. caerulea is more or lessrestricted to heathland areas and pine plantations. Mol-inia caerulea forms swards or large tussocks from 8to 20 cm (sometimes .30 cm) in diameter at the base.It has an enormous root system that forms a densetangle at the top and that penetrates to a great depth(.100 cm; Aerts 1993). Because of its large root sys-tem, the species is well adapted to survive intense fires.

In contrast to many other grass species, the tuftedgrowth form shows very little lateral vegetative spread,making spatial spread and colonization of vacant siteshighly dependent on sexual reproduction and seed set.Flowers are wind pollinated and seeds are dispersed bywind. Mean seed production per plant is generally high(.20 000 seeds per flowering plant; Bruggink 1993,Brys et al. 2005). Seeds are relatively small, have amean air-dry mass of 0.53 mg (Grime et al. 1981), andthey are readily able to colonize bare ground (Tayloret al. 2001).

Study site

This study was carried out at the Kalmthoutse Heide,a relatively large heathland area (1020 ha) situated inthe northern part of Belgium (near Antwerp). The soiltype can be characterized as a humus podsol. An in-tense and large fire on 24 April 1996 burned nearlyone-third of the area (see Plate 1). Before the fire hadburned the area, the vegetation at the study site wascharacterized by relatively high dominance of Callunavulgaris, whereas M. caerulea occurred in isolated tus-socks. Other plant species occasionally observed wereErica tetralix, Rynchospora alba, Festuca ovina subsp.tenuifolia, Carex pilulifera, and the mosses Campy-lopus introflexus, Cladonia portentosa, Cladonia floer-keana, and Hypnum jutlandicum. By the year followingthe fire, burned M. caerulea plants had resprouted andproduced seeds.

Seed dispersal distances

Seed dispersal distances were determined indirectlyby investigating spatial distribution patterns of viableseeds in the soil. Therefore, the upper part of the soil(5 cm) was sampled around 16 mature individuals,

December 2005 2099FIRE AND INVASIVE SPREAD OF TUSSOCK GRASS

PLATE 1. The high-intensity fire that in April 1996 destroyed almost one-third of the Kalmthoutse Heide. Photo credit:Marc Slootmackers.

eight in burned and eight in unburned heathland. AsM. caerulea has only a shallow seed bank and samplingtook place in November (i.e., one month after seed set),the sampled seeds almost certainly originated from thecurrent year’s seed set. This method was preferredabove the seed trap method, because M. caerulea pro-duces large amounts of unviable seeds (due to smutfungus and post-dispersal seed predation; R. Brys, per-sonal observation), which may lead to overestimationof seed dispersal distances.

For each individual, several soil cores were taken atthe main angles (08, 908, 1808, and 2708) and at regulardistances from the parent plant (0–50 cm, 50–100 cm,100–200 cm, 200–300 cm, and 300–400 cm). Soilcores were taken with a soil bore with a diameter of3.5 cm. For each angle and each interval, soil sampleswere regularly spaced within the different intervals.After collection, soil cores were washed through acoarse (4 mm mesh width) and fine (0.2 mm meshwidth) sieve. The concentrated samples were spreadout into a layer of maximum 2 mm thickness on 15 315 cm trays filled with sterilized potting soil. Seedswere germinated in laboratory conditions (16 h day-light, 258C; 8 h dark, 168C) for six weeks, after whichgermination had ceased. For each individual and foreach distance class, soil cores were pooled to obtain

mean seed densities at particular distances from theparent plant.

Demographic data and constructionof projection matrices

In 1997, eight 2 3 2 m2 permanent monitoring plots(four in burned and four in unburned heathland) wereestablished. Based on soil and vegetation maps (DeBlust and Slootmaekers 1997) and aerial photographs,it was ascertained that the study was performed on alarge, homogenous site that showed no differences insoil conditions and vegetation characteristics prior toburning. Plots were laid out in pairs (one in burnedand one in unburned heathland), which allowed inves-tigation of the importance of local site conditions onthe effects of fire on population dynamics. From 1997until 2000, all plants within each plot were monitoredannually in late September. At that time, seedlings hademerged and were clearly visible. Individual plantswere not tagged, but mapped using a 10 3 10 cm2;grid. In this way, the fate of each individual was re-corded in each plot in each year. At the same time,basal diameter of adult, seed-producing plants was alsorecorded.

A biological stage classification based on plant sizeand reproductive status was used to classify each M.


FIG. 1. Life cycle graph of Molinia caerulea and the as-sociated population projection matrix. Arrows represent tran-sitions between stages, and letters show the connection be-tween each transition and its corresponding matrix entry. Ma-trix entries are subdivided in fecundity (F, number of seed-lings per reproductive adult), growth (G, transition to higherstages), and survival (S, remaining at the same stage or ret-rogression to a lower stage).

caerulea individual into one of five classes: seedlings(Sdl), juveniles (J), small reproductive plants with ro-sette diameter ,12.5 cm (R1), medium-sized repro-ductive plants with rosette diameter 12.5 to ,25 cm(R2), and large reproductive plants with rosette di-ameter .25 cm (R3). Seedlings were defined as firstyear vegetative plants, whereas juveniles consisted ofall nonseedling vegetative plants older than one year.The life cycle graph of M. caerulea is represented inFig. 1.

Transition matrices were constructed from these datafor each plot in each year. The ‘‘anonymous reproduc-tion method’’ (Caswell 2001) was used to estimatestage-specific fertility. Therefore, the total number ofseedlings in year t 1 1 was multiplied by the proportionof viable seeds produced by each stage in year t. Bothfor plants from burned and unburned plots, plant size(basal diameter) was significantly related to seed pro-duction (one-way ANOVA, F 5 12.76, P , 0.001 andF 5 6.38, P 5 0.004 for plants from burned and un-burned plots, respectively).

Data analysis

Averaged demographic matrices rather than the in-dividual matrices were used to determine populationgrowth rate and invasion speed. Each averaged matrixwas a weighted mean of the matrices for all the plot-year combinations corresponding to that plot. Follow-ing Caswell and Kaye (2001), the weight for all ele-ments within a column was the sample size from whichthat column was estimated. From these matrices, wecalculated the asymptotic growth rate, l, followingmethods outlined in Caswell (2001).

In order to assess whether fire affected populationgrowth rates, a nonparametric randomization procedurebased on permutations of individual life history wasused. Since plots were sampled in pairs (one in burnedand one in unburned heathland), for each pair individ-ual life histories were randomly permuted between theburned and unburned plot, new matrices were con-structed, and the population growth rate was calculated.This procedure was repeated 2000 times to obtain afrequency distribution of population growth rates underthe null hypothesis of no difference between burnedand unburned plots. Finally, the observed growth ratewas compared with those obtained by randomly per-muting individuals.

Elasticity analysis was conducted to determine lifecycle transitions that have the largest impact on l (deKroon et al. 1986). Following Parker (2000), elastic-ities were summed for each column, excluding fecun-dity, to generate composite elasticities for the fate ofseedlings, juveniles, and small, medium, and large re-productive adults. Additionally, a composite elasticityfor fecundity was also generated. In this way, the elas-ticity structure for burned and unburned plots was rep-resented.

Invasion speed was obtained following methods out-lined in Neubert and Caswell (2000). To briefly review,this model assumes that population spread is the netresult of two processes: population growth and dis-persal. Assume that we have divided the populationinto m life history stages. Let ni(y, t) be the populationdensity of stage i at location y and time t, and let bij(n1(y,t), n2(y, t), . . . nm(y, t)) be the per capita production ofstage i individuals at time t 1 1 by stage j individualsat time t. Finally, let kij(x 2 y)dx be the fraction ofstage i individuals produced by stage j individuals aty that disperse into the interval (x, x 1 dx). If there isno dispersal during a given transition, the associatedkernel is the Dirac delta function d(x 2 y), a functionthat (very roughly speaking) is zero if x ± y, is infinitewhen x 5 y, and integrates to 1. That is, with probability1, such an individual stays where it is.

For each stage i, we then have

n (x, t 1 1)i

` m

5 k (x 2 y)b [n (y, t), . . . , n (y, t)]n (y, t) dyOE i j i j 1 m jj512`

(1)

or in matrix notation


`

n(x, t 1 1) 5 [K(x 2 y) + B ]n(y, t) dy. (2)E n(y,t)2`

The symbol ‘‘+’’ stands for the Hadamard product(Horn and Johnson 1985), wherein multiplication iscomputed element by element. For M. caerulea, weassumed that K had the form

d(x) d(x) k(x) k(x) k(x)

d(x) d(x) d(x) d(x) d(x) K(x) 5 d(x) d(x) d(x) d(x) d(x) . (3)

d(x) d(x) d(x) d(x) d(x) d(x) d(x) d(x) d(x) d(x)

That is, we assumed that dispersal only occurred di-rectly after the production of seeds by adults, and thatthe dispersal kernel was the same for all transitions.

Under biologically reasonable conditions on the ma-trix Bn (including nonnegativity, primitivity, and theabsence of Allee effects [Lui 1989, Neubert and Ca-swell 2000]), the rate of spread of the population isgiven by

1c* 5 min log r (s) (4)1[ ]ss.0

where r1(s) is the largest eigenvalue of the matrix M(s)+ A, A 5 B0, and the i, j element of the matrix M(s)is the moment generating function of the kernel kij(x),i.e.,

`

sxm (s) 5 k (x)e dx. (5)i j E i j2`

We use s* to denote the value of s that produces theminimum in (4).

The sensitivity of the rate of spread, c*, to changesin the entries of A is given by (Neubert and Caswell2000):

m (s*) v w]c* i j i j5 (6)

]a s*r ^v, w&i j 1

where ^·& denotes the scalar product, r1 is the dominanteigenvalue of the matrix A + M(s*), and w and v arethe corresponding right and left eigenvectors of A +

M(s*). Elasticities are calculated as

a ]c*i j . (7)1 21 2c* ]aij

The expressions given in (1)–(7) refer to a modelthat is set in a one-dimensional space, but the dispersaldata were collected in two spatial dimensions. Sincedispersal distances were pooled into discrete classeswithout regard for direction, we assumed that dispersalwas radially symmetric and hence that the rate of spreadwas the same in every direction. Thus the measureddispersal kernels were two-dimensional histograms ofthe following form:

f if r , r , ri i21 ik (r) 5 (8)2 50 otherwise

where r 5 , 1 # i # ,, and the ri are the2 2Ïx 1 yhistogram bin edges. The appropriate one-dimensionalkernel to use in formula (3) for this two-dimensionalkernel is the marginal distribution:

`

2 2k(x) 5 k (Ïx 1 y ) dy. (9)E 22`

Lewis et al. (2005) have shown that the associated mo-ment generating function is given by

,2pm(s) 5 f [r I (sr ) 2 r I (sr )] (10)O i i 1 i i21 1 i21s i51

where I1 is the modified Bessel function of the firstkind and first order (Abramowitz and Stegun 1970).

Invasion speed was calculated for each plot in burnedand unburned heathland using their associated dispersalkernels and population projection matrices. Finally, inorder to study the impact of fire on the relative im-portance of dispersal and demographic parameters indetermining invasive spread of M. caerulea, dispersaland demographic parameters were combined in everypossible way, and for each combination of parametersinvasion speed was calculated for each plot separatelyand for the average demographic matrix across the foursites. All calculations were performed in MATLAB,Version 6.5. (MathWorks, Natick, Massachusetts,USA)

RESULTS

The seed dispersal distributions obtained from thegermination experiment are shown in Fig. 2. Mostseeds fell in the immediate neighborhood of the parentplant and only a very small fraction of seeds traveledfurther than 4 m. Although seedling densities aroundparent plants were almost twice as high in the burnedcompared to the unburned site, the associated dispersalkernels showed very little differences (Fig. 2).

A total of 5111 individuals were monitored duringthe 4-yr period. All populations (n 5 8) were increas-ing. Population growth rates (l) calculated from theaveraged matrices (Appendix A) varied between 1.773and 2.561 (mean 5 2.255, SD 5 0.378) in the burnedplots and between 1.177 and 1.311 (mean 5 1.237, SD

5 0.055) in the unburned plots (Fig. 3). For all sites,permutation tests revealed that growth rates were sig-nificantly larger in burned compared to unburned plots(P , 0.001).

Elasticity analysis showed that in the burned situa-tion the life cycle stage that is most important in re-lation to its contribution to population growth rate wasgrowth of juveniles to reproductive adults, whereas inthe unburned plots survival of the largest individualswas most influential to population growth rate (Ap-pendix B). The elasticity structure also differed largely


FIG. 2. Histograms of seedling densities at different distances from parent plants based on the seed germination experimentand the associated dispersal kernels.

FIG. 3. Population growth rates calculated from the av-eraged population matrices of Molinia caerulea in four plotsthat were burned and four plots that were unburned (see Meth-ods: Data analysis).

FIG. 4. Composite elasticities for fecundity and the fateof each stage for burned plots (open circles) and unburnedplots (solid triangles). Error bars represent the standard devi-ation of four plots. Elasticities were combined by summingeach column, excluding fecundity. Abbreviations: Fec, fecun-dity; Sdl, seedling; Juv, juvenile; R1, small reproductive adult;R2, medium reproductive adult; R3, large reproductive adult.

between burned and unburned plots (Fig. 4). The com-posite elasticities for fecundity and the seedling stagewere, on average, two times larger for burned than forunburned plots (22% vs. 10%, respectively). Compos-ite elasticities for reproductive adults, on the otherhand, were much larger in the unburned than in theburned populations.

Invasion speed (c*) ranged from 0.5916 to 0.8502m/yr (mean 5 0.7518, SD 5 0.1141) in burned plotsand from 0.2291 to 0.3034 m/yr (mean 5 0.2606, SD

5 0.0311) in unburned plots (Fig. 5). When combining

dispersal kernels and population projection matricesfrom burned and unburned plots, it appeared that dis-persal parameters were far less influential in determin-ing invasive rates than demographic parameters (Table1), as there was only an average increase of 2% ininvasion speed when, irrespective of demographic pa-rameters, dispersal kernels in unburned plots were re-placed by dispersal kernels obtained in burned heath-


FIG. 5. Invasion speed, c*, for Molinia caerulea in burnedand unburned heathland using dispersal kernels of Fig. 2.

TABLE 1. Invasion speed, c*, of Molinia caerulea calculatedfrom dispersal and demographic parameters of plots locatedin burned and unburned heathland at four sites.

Dispersal

Demography

Unburned Burned

UnburnedSite 1 0.2519 0.7413Site 2 0.2291 0.5813Site 3 0.2581 0.8015Site 4 0.3034 0.8382ADM† 0.3072 0.7866

BurnedSite 1 0.2576 0.7541Site 2 0.2350 0.5916Site 3 0.2641 0.8128Site 4 0.3097 0.8502ADM† 0.3139 0.7986

Notes: Demographic parameters refer to the time-averagedtransition matrices calculated for each pair of plots (one inburned heathland, one in unburned heathland). In total, fourpairs of plots were studied. Dispersal parameters refer to thedispersal kernel calculated for plants located in burned andunburned heathland, respectively (see Methods: Data analysis).

† Invasion speed calculated from the average demographicmatrix (ADM) across the four sites.

land. On the other hand, invasion speed dramaticallyincreased when projection matrices from unburnedheathland were replaced by those from burned heath-land (Table 1).

Sensitivity matrices for M. caerulea in burned andunburned heathland show that in both cases invasionrate was most sensitive to changes in the transitionsfrom seeds to large-class reproductive adults (Fig. 6).The elasticity matrix, on the other hand, shows that,on average, the largest proportional changes in invasionrate in burned plots are generated by changes in thegrowth of seedlings to juveniles and of juveniles tosmall-sized adults in burned plots. In unburned plots,however, there is no particular life cycle or transitionthat overwhelmingly dominates c*, as elasticities arefairly uniformly distributed throughout the life cycle(Fig. 6). Compared to burned plots, survival of repro-ductive adults appeared to be more important in un-burned plots.

As seen in Fig. 2 and Table 1, dispersal kernels didnot significantly differ between the burned and un-burned situation. Demographic parameters, however,did change (Appendix A), and it is this change in de-mography that is primarily responsible for the differ-ences in the computed invasion rates. We therefore useda life table response experiment (LTRE) analysis todecompose the difference between invasion speeds ofburned and unburned sites into contributions from dif-ferences in the entries in A. The average demographicmatrix in unburned years is

0 0 0.4485 4.1658 6.3630 0.4933 0.5395 0 0 0

(u)A 5 0.0100 0.2998 0.7285 0.1415 0 0 0.0070 0.2070 0.6123 0.0278 0 0 0 0.2253 0.9722

(11)

and in burned years is

0 0 6.5055 17.4755 52.4338 0.7993 0.0410 0 0 0

(b)A 5 0.0288 0.6568 0.3808 0 0 . 0 0.0078 0.5388 0.4915 0 0 0 0.0303 0.4993 1.0000

(12)

Using an average dispersal kernel estimated from bothburned and unburned years in conjunction with thesetwo matrices gives c(u) 5 0.3117 m/yr as the projectedinvasion speed in the unburned situation and c(b) 50.7947 m/yr as the speed after burning. The first-orderapproximation to the difference in wave speed can bewritten as follows (Caswell et al. 2003):

]c(b) (u) (b) (u)c 2 c ø [a 2 a ] (13)O i j i j )]ai,j (b) (u)i j [A 1A ]/2

and the matrix of contributions from the demographicdifferences is given by

]c(b) (u)[A 2 A ] + 1 2]aij

0 0 0.1366 0.0513 0.0413 0.0599 20.0240 0 0 0

5 0.0194 0.0907 20.0209 20.0015 0 . 0 0.0005 0.0522 20.0032 20.0002 0 0 0.0104 0.0161 0.0004

(14)

From this matrix, it can be concluded that the burned


FIG. 6. Sensitivity and elasticity matrices of invasion speed, c*, to changes in aij for four plots in burned and four plotsin unburned heathland. Rows and columns correspond to the matrix in Fig. 1 (see also Neubert and Caswell 2000).

population has an advantage in reproduction and re-cruitment (growth of seedlings and juveniles).

DISCUSSION

During the last decades, M. caerulea has invaded largeareas of heathland in Western Europe (e.g., Hansen1976, Berendse et al. 1994, Chambers et al. 1999). Atpresent, the species is considered a major threat to heath-

land conservation. Previous research (Grant et al. 1963,Todd et al. 2000, Marrs et al. 2004) had already sug-gested that fire had a beneficial impact on M. caerulea,but until now a mechanistic explanation for the increasedabundance of M. caerulea after fire had not been pro-vided. Using information on both dispersal distances anddemography allowed us to assess the impact of fire oninvasive spread of M. caerulea in dry heathland.


FIG. 6. Continued.

Dispersal

The spatial distribution of seeds about parent plantswas typically leptokurtic. Distances traveled by mostM. caerulea seeds were quite small as the mean dis-persal distance was found to be ,1 m. These resultsare in accordance with seed dispersal distances foundfor other grass species. For example, the mean seeddispersal distance of the perennial tussock grass Hy-parrhenia diplandra was also around 1 m (Garnier andDajoz 2001b, Garnier et al. 2002). Similar seed dis-

persal distances as the ones observed for M. caeruleawere also reported by Guardia et al. (2000) for thetussock forming grass Achnatherum calamagrostis andby Watkinson et al. (2000) for the annual grass Vulpiaciliata, respectively. Surprisingly, although mean totalseed output per plant in the burned situation was nearlythree times higher than in the unburned situation (Bryset al. 2005) and notwithstanding the fact that fire pro-voked sizeable increases in seedling densities, seedproduction hardly affected seed dispersal distances.


Hence, the results point to low overall seed dispersalof M. caerulea both in burned and unburned heathland.

Demographic changes following fire

Although all the matrices analyzed gave projectedrates of increase larger than one, indicating that M.caerulea populations increased both in unburned andburned heathland, population growth rates were, onaverage, two times higher in burned compared to un-burned plots. This clearly demonstrates that fire has apronounced, positive effect on the demography of M.caerulea. In line with the results presented here, Grantet al. (1963) and Todd et al. (2000) also observed thatburning favored M. caerulea in British moorlands. Inboth cases, the species was found to rapidly recoverafter burning. Studies on other grass species have alsoshown beneficial effects of fire on population demog-raphy (e.g., Silva et al. 1991). Canales et al. (1994)even found growth rates that were four times larger inburned plots compared to unburned plots for the annualgrass Andropogon brevifolius.

The much higher elasticities for fecundity andgrowth of the seedling stage in the burned comparedto the unburned plots clearly demonstrate that fire in-duced a significant increase in seed germination andsurvival rates of M. caerulea. Indeed, two years afterfire seedling recruitment was nearly six times higherin burned plots than in unburned plots and after fouryears seedling recruitment was still significantly higherin burned than in unburned heathland (results notshown). This can be explained in part by increasedgermination rates of seeds originating from plantsgrowing in burned sites and in part by the increasedseed production after fire (Brys et al. 2005). Further-more, burning and the associated decrease in litter andincrease in light penetration to the soil (Todd et al.2000) may have created ideal conditions for germi-nation. Despite higher seedling and juvenile densities,these conditions also resulted in lower mortality ratesof seedlings and juveniles (data not shown). Using 10years of demographic data, Menges and Quintana-As-cencio (2004) found similar decreases in compositeelasticities for the seedling stage with time since fire,and increases in elasticities for stasis of the largestreproductive individuals.

Spatial spread

Although data on the spread of perennial tussockgrass species are still rare, most studies assume initialseedling recruitment followed by prolonged vegetativereproduction (Suzuki et al. 1999). MacDonald and Lief-fers (1991), for example, found extensive genetic var-iation in the perennial grass Calamagrostis canadensis,but no evidence for seedling recruitment was observed.In contrast, M. caerulea showed repeated seedling re-cruitment, which resulted in spatial spread of the spe-cies. Recent studies on other tussock grass species (e.g.,Achnatherum calamagrostis [Guardia et al. 2000] and

Festuca rubra [Suzuki et al. 1999]) have reported sim-ilar results, indicating the importance of sexual repro-duction in determining spatial spread of these grassspecies.

Furthermore, the results of this study have clearlyshown that disturbances such as fire may largely affectinvasive spread of plant species. This may be causedby altered dispersal distances, changes in vital rates,or both. In the case of M. caerulea, fire increased thespreading speed of M. caerulea by a factor of three.This was mainly the result of changes in demographicparameters rather than changes in dispersal parameters.Caswell et al. (2003) already demonstrated that dif-ferences in demography could be as important as dif-ferences in dispersal in determining invasion speed.Increased seed production, germination, and growth ofseedlings and juveniles were the main factors contrib-uting to the observed differences in invasion spreadbetween burned and unburned plots, as the LTRE anal-ysis clearly showed positive contributions for these lifecycle transitions. Moreover, elasticity analysis of in-vasion speed pointed to fecundity and growth of seed-lings as important determinants of invasive spread ofM. caerulea after fire. Hence, our results point to sexualreproduction and repeated seedling recruitment as themain factors driving spatial spread of the species afterfire.

Implications for conservation

One of the primary motivations of this study was tounderstand the rate of spread of M. caerulea in dryheathland communities and the factors influencing thisspread in order to formulate management actions aim-ing to halt future invasions of the species. Analysis ofinvasion speed in both burned and unburned sites clear-ly demonstrated that large, unintended fires like theone studied here are detrimental for heathland conser-vation, as this fire clearly affected invasion spread ofM. caerulea. In the long term, this may lead to absolutedominance of Molinia as the high productivity afterfire (Brys et al. 2005) leads to higher litter production,which in turn may lead to a further competitive ad-vantage of M. caerulea and increased fire probabilitiesdue to the increased aboveground fuel availability. Giv-en the observation that fire regimes are expected tochange over the next decades in response to globalwarming and land use changes (e.g., Flannigan et al.2000, Pausas 2004), this may have serious implicationsfor heathland conservation. The Kalmthoutse Heidemay be exemplary, since during the last three decadesat least three large and intense fires (1976, 1996, and1997) have burned substantial areas of the KalmthoutseHeide and have led to an increased abundance of Mol-inia. A similar increase in fire frequency has also beenobserved in other heathland areas in Belgium.

These observations urge for an absolute necessity toreduce the probability of future fires by decreasing litteraccumulation and hence aboveground fuel build-up.


Recent research has shown that the latter can be bestachieved by grazing in late summer or by selectiveherbicide application (glyphosate; Milligan et al. 2003,Marrs et al. 2004). Further, the results of this studyalso cast doubt on the possible role of controlled burn-ings in reducing M. caerulea cover in heathlands. Pre-vious research (Grant et al. 1963, Todd et al. 2000) hasalready suggested that burning was not effective incountering expansion of M. caerulea. In case a fire hasburned large areas of heathland, it is absolutely nec-essary to reduce seed set after fire, as fecundity andgrowth of seedlings and juveniles were by far the mostimportant determinants of invasive spread. This can beachieved by mowing down all seed producing plantsbefore seed set. In this way, germination rates can bekept low, and invasion can be halted. The fact that,four years after burning, germination rates in burnedheathland were still significantly higher than in un-burned heathland indicates that at least several yearsof active management are required to halt invasion ofthe species after fire.

ACKNOWLEDGMENTS

The authors thank K. Molenberghs for permission to carryout all fieldwork at the Kalmthoutse Heide, and H. Caswelland C. Hunter for helpful discussions. Two anonymous re-viewers provided useful comments on an earlier version ofthis manuscript. This work was supported by the FlemishFund for Scientific Research (FWO) to HJ, the U.S. NationalScience foundation (DEB-0235692, OCE-0083976), and theU.S. Environmental Protection Agency (R-8290891) toMGN. This manuscript is Woods Hole Oceanographic Insti-tution contribution 11314.

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APPENDIX A

A table showing the averaged transition matrices for each site in burned and unburned heathland is available in ESA’sElectronic Data Archive: Ecological Archives A015-063-A1.

APPENDIX B

A table showing the elasticity values of averaged population projection matrices of four sites in burned and four sites inunburned heathland is available in ESA’s Electronic Data Archive: Ecological Archives A015-063-A2.

FIRE INCREASES INVASIVE SPREAD OF MOLINIA CAERULEA MAINLY THROUGH CHANGES IN DEMOGRAPHIC PARAMETERS

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