Population ecology and conservation status of the last naturalpopulation of English yew Taxus baccata in Denmark

Jens-Christian Svenninga,*, Else MagaÊ rdb

aDepartment of Systematic Biology, University of Aarhus, Herbariet, bygn. 137, Universitetsparken, DK-8000 Aarhus C, DenmarkbDepartment of Genetics and Ecology, University of Aarhus, Universitetsparken, DK-8000 Aarhus C, Denmark

Received 28 May 1998; received in revised form 22 August 1998; accepted 24 August 1998

Abstract

English yew Taxus baccata L. has become extinct or rare in many parts of Europe. Here we investigate the status of the only

natural population persisting in Denmark. While many other yew populations are declining, the Danish population increased from<200 individuals in 1925 to >2000 in 1998. This was most likely due to the thinning of the tree stand at this site, as reproductiveactivity, strobilus production, and recruitment were enhanced at better lit microsites. The declining status of other populations isprobably often caused by succession from open woodland to dense forest. The light dependency is consistent with the Quaternary

history of yew. The sex ratio of the Danish yew population was female-biased, probably due to chance. Yew invaded forest areasneighbouring source populations at rates of 43 m yrÿ1, but forest management impeded this process. # 1999 Elsevier Science Ltd.All rights reserved.

Keywords: Forest management; Taxus baccata; Tree recruitment; Understorey light availability; Yew decline

1. Introduction

During the last 5000 years human land-use hasreduced the area of temperate forest in Europe andchanged the structure and species composition of theremaining fragments (e.g., Aaby, 1986; Broekmeyer andVos, 1993; Ellenberg, 1988; Jahn, 1991; Moore, 1996;Peterken, 1996). One of the European tree species whichhas been most negatively a�ected by this process isEnglish yew Taxus baccata L., a dioecious gymnospermranging in size from an understorey shrub to a 20±32.5m tall tree (Krol, 1978; Milner, 1992; Tutin et al., 1964).Yew has a stress-tolerant life strategy sensu Grime beingslow-growing, slow to reach maturity (c. 70 years), long-lived (>1000 years), shade-tolerant, and producingstrong decay-resistant wood (Brzeziecki and Kienast,1994). It occurs in temperate Europe north to 63�N andeast to Estonia and White Russia and in western Asiaand northern Africa (e.g., Czatoryski, 1978b; Lewan-dowski et al., 1995; Nùrrevang and Lundù, 1980;O'Connell et al., 1987; PenÄ alba, 1994; Sarmaja-Korjo-nen et al., 1991; Tittensor, 1980; Tutin, 1953; Watts et

al., 1996). While its natural distribution is wide, yew hasbecome locally extinct or reduced to small isolatedpopulations in many parts of Europe during the last4000 years (Czatoryski, 1978b; Lewandowski et al.,1995; Nùrrevang and Lundù, 1980; PenÄ alba, 1994; Sar-maja-Korjonen et al., 1991; Tittensor, 1980; Tutin,1953; Watts et al., 1996). In Denmark, only one yewpopulation has survived (Nùrrevang and Lundù, 1980,1981; Worsùe, 1985). Archaeological evidence andtoponyms indicate a more widespread distribution inDenmark until 1±2000 years ago (Nùrrevang andLundù, 1981), although yew has only been sporadicallyrecorded in Danish postglacial pollen diagrams (Aaby,1986; Andersen, 1989).

The main reasons for the decline of yew are wide-spread deforestation, selective felling of yew, and graz-ing (Bugala, 1978; Czatoryski, 1978b; Jahn, 1991;Nùrrevang and Lundù, 1980; Tittensor, 1980; Tutin,1953). Yew is very sensitive to grazing by livestock (e.g.,Mitchell, 1988, 1990a; Sarmaja-Korjonen et al., 1991),probably contributing much to restricting its range(Mitchell, 1990b). It can be deadly to horses, and to alesser extent also to cattle and sheep, but the toxicitydisappears when these animals have constant accessto yew foliage (HñggstroÈ m, 1990; Williamson, 1978).

BIOLOGICAL

CONSERVATION

Biological Conservation 88 (1999) 173±182

0006-3207/99/$Ðsee front matter # 1999 Elsevier Science Ltd. All rights reserved.

PII: S0006-3207(98)00106-2

* Corresponding author. Tel.: +45 8942 2742; fax: +45 8613 9326;

e-mail: jens-christian.svenning@biology.aau.dk.

Selective felling of yew has occurred for its strong woodand bast, but also because of its toxicity, for ornamentalpurposes, and because foresters regarded it as a weed(Bugala, 1978; Czatoryski, 1978b; Ellenberg, 1988;Helms, 1925; Milner, 1992; Nùrrevang and Lundù,1980; Sarmaja-Korjonen et al., 1991; Tittensor, 1980;Worsùe, 1985). Recently, other taxads have also declineddue to forest degradation and selective harvesting forextraction of the anticancer compound taxol from thebark (Busing et al., 1995; Kral, 1983; Nemecek, 1996).

Many extant natural populations of English yew,from England to the Caucasus, are threatened by poorrecruitment (Czatoryski, 1978a; Hulme, 1996; Krol,1978; Lewandowski et al., 1995; Pridnya, 1984; Titten-sor, 1980). The lack of regeneration in many popula-tions is intriguing as self-seeding from garden plants iscommon and successful regeneration occurs in othernatural populations in the same regions (Bartkowiak,1978; Krol, 1978; Stace, 1997). The causes of this lack ofregeneration are poorly known, but herbivory by deer isinvolved in some areas. T. baccata is very susceptible tobrowsing and bark stripping by deer (HñggstroÈ m, 1990;Kelly, 1981; Sarmaja-Korjonen et al., 1991), and strongnegative e�ects on recruitment and adult survival hasbeen reported from areas with dense deer populations(HñggstroÈ m, 1990; Kelly, 1981; Mitchell, 1988; Wil-liamson, 1978). Similarly, T. canadensis Marsh. isdeclining in abundance in the Great Lakes region due toheavy deer browsing (Gill et al., 1995). In England,rabbit grazing and seed predation by rodents are alsoknown to be involved in the lack of recruitment (Hulme,1996; Watt, 1926).

Apart from herbivory several other factors have alsobeen suggested as responsible for the declining status ofmany yew populations: (1) competition for light withtaller-statured deciduous trees, notably the highlyshade-giving beech Fagus spp. (Czatoryski, 1978a; Krol,1978; Pridnya, 1984); (2) adverse soil conditions, eitherdue to soil pathogens, autotoxicity, or changed abioticconditions (Krol, 1978; Lewandowski et al., 1995; Mil-ner, 1992); and (3) loss of genetic variation (Lewan-dowski et al., 1995). The last factor has been rejected asa strongly declining population in Poland exhibited highlevels of genetic variability (Lewandowski et al., 1995).

Here, we report on the ecology and conservation ofyew with focus on the only natural Danish populationstill persisting (Nùrrevang and Lundù, 1980, 1981;Worsùe, 1985). The four topics that we investigate are:(1) whether this population has increased or decreasedin size since it was last censused (Helms, 1925), andwhether recruitment is failing as has been reported fromother sites; (2) if light availability in¯uenced strobilusproduction and recruitment, as implicated by thehypothesis that competition for light with taller-statureddeciduous trees is responsible for the declining status ofmany yew populations. In the light of our results, we

also discuss the Quaternary history of yew and the otherfactors potentially involved in the yew decline; (3) if andhow fast yews were recolonizing the forest areas neigh-bouring source populations; and (4) how forest man-agement has a�ected the Munkebjerg population, andhow forest management in¯uenced yew recolonization.For investigating questions 3±4 we included an addi-tional Danish study site.

2. Methods

2.1. Study areas

The main study site was the forest MunkebjergStrandskov (55�410 N, 9�370 E) in Jutland, Denmark(Fig. 1). It is an 800 ha forest situated in hilly terrainwith steep slopes, 0±93 m a.s.l. (Anonymous, 1982;Mùller and Staun, 1995). The soil is mainly clay, butglacial sand occurs on some slopes and ridges (Mùllerand Staun, 1995). The forest is a mosaic of managedbeech forest Fagus sylvatica L. and conifer plantations.A description of the ¯ora can be found in Gravesen(1986).

The yew population which occurs in a gully in thenortheastern corner of the forest was discovered in 1865and has been protected by law since 1933 (Nùrrevangand Lundù, 1980; Worsùe, 1985). At the time of dis-covery most individuals were of low stature andstrongly damaged by cutting, whereas now the popula-tion contains many large and healthy individuals

Fig. 1. Map of Denmark showing the location of the two study sites,

Munkebjerg Strandskov (1) and Marselisborg Skov (2).

174 J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182

(Helms, 1925; Worsùe, 1985). Most yews occur within 3ha of sandy slopes and plateaus and a clayey poorlydrained gully bottom. The canopy is dominated bybeech, and much of the canopy is open due to thinningof the tree stand. Holly Ilex aquifolium L. is common,and the ground ¯ora is dominated by Luzula sylvatica(Hudson) Gaudin, Vaccinium myrtillus L. and mosseson the sandy slopes and plateaus, and Hedera helix L.and Anemone nemorosa L. in the gully bottom. Werecorded all yews in a 0.16 ha plot in the centre (coreplot) and a 0.35 ha plot at the edge of the yew popula-tion (edge plot) on the area of sandy slopes and plateausas well as in a 0.10 ha plot in the gully bottom (bottomplot). We also recorded all yew saplings and adultsfound along 6 km of trails in the surrounding forest.The yews at Munkebjerg were also studied in 1925 byHelms (1925) who estimated the population size,described the general health and distribution of thepopulation, and measured height and girth of the largestindividuals.

The second site (Fig. 1), the wood Marselisborg Skov(56�080 N, 10�120 E) is on level ground, 0±16 m a.s.l.(Anonymous, 1982), and clayey soil. It is intensivelymanaged and the canopy is dominated by beech, and inparts also by oak Quercus robur L. In the herb layer,Mercurialis perennis L., Anemone nemorosa, andRanunculus ®caria L. are common, while Ilex aquifoliumoccurs only as scattered, small individuals. The forest,enclosed in the city of Aarhus, is bordered by gardensand parks. Inside the forest, scattered small yews occur,none exceeding 2.5 m in height. These are self-sownfrom the numerous reproductive yews planted in the oldgardens just north of the forest. We recorded all yews ina 9.5 ha section of the forest.2.2. Field recordings

In February±March 1998, all individuals in the studyareas were censused. All stems for which an extantconnection to another stem could not be establishedwere recorded as separated individuals following Helms(1925). For each individual we recorded diameter atbase, sex (fertile individuals only), reproductive status(fertile or completely sterile), strobilus production (0,1±5, 6±10, 511 strobili per shoot, where 0 for fertile

individuals corresponds to an average of <1 strobilusper shoot), and understorey illumination index (Table 1).Exposure was judged at 1.80 m height vertically above/below the crown of the individual, excluding the foliageof the individual itself from consideration. Small gapswere canopy gaps about 1±9 cm in maximum diameteras measured on a centimeter scale held 20 cm away(using a measured string) from and parallel to the eyesof the observer. Medium, large, and very large gapswere de®ned likewise as being 10±13, 14±29, and 530cm in maximum diameter, respectively. We also mea-sured the diameter at 1.30 m height (DBH) of three verylarge individuals within the main yew population atMunkebjerg. One of these was also measured by Helms(1925). We were not able to precisely locate the othermajor yews measured by Helms. Thus, his other mea-surements could not be used in the analyses. At theMarselisborg Skov site and along the Munkebjerg trailsthe location of each yew was also mapped. In Mar-selisborg Skov, we also mapped the distribution ofdense and open understorey. Dense understorey wasde®ned as areas were tree saplings and shrubs formedthickets, di�cult to penetrate.

2.3. Data analysis

Following Hulme (1996), seedlings, saplings, andadults were de®ned by the following diameter limits: <5mm, 55 mm but <30 mm, and 530 mm, respectively.Sometimes reproduction began at 4±5 mm, but we usedHulme's terminology for comparability. The illumina-tion index (Table 1) was condensed to a binary index ofdense canopy (illumination index 1.0±2.0) and opencanopy (52.5) in the logistic regression and G-testanalyses.

Reproductive status and sex were analyzed againstdiameter and canopy openness by nominal logisticregression, while strobilus production (only consideringfertile individuals) was analyzed against diameter, sex,and canopy openness by ordinal logistic regression.Logistic regressions were done using the JMP 3.2.2 sta-tistical package (SAS Institute Inc.). All other analyseswere done by standard G-tests, Wilcoxon's two-sample

Table 1

Understorey illumination index. Modi®ed from Clark and Clark (1992) and Clark et al. (1993)

Score De®nition

5.0 Completely exposure within the smallest 90� inverted cone that completely encompasses the crown

4.0 590% vertically exposure, but somewhat blocked within the 90� cone3.0 10±90% vertical exposure

2.8 <10% vertical exposure; exposed to at least one very large or 52 medium large lateral gaps

2.5 <10% vertical exposure; exposed to at least one large or 52 medium lateral gaps

2.0 <10% vertical exposure; exposed to at least one medium or 52 small lateral gaps

1.5 <10% vertical exposure; exposed to one small lateral gap

1.0 Not exposed even to a small lateral gap

Exposure was judged at 1.80 m height. For further details, see Section 2.2.

J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182 175

test, or Kruskal±Wallis one-way ANOVA. All singleclassi®cation goodness of ®t tests were done using Wil-liam's correction (Sokal and Rohlf, 1995).

3. Results

3.1. Population size

Yew densities at Munkebjerg are given in Table 2.The areas represented by the core, edge, and bottomplot were 0.90, 0.75, and 1.46 ha, respectively. Thus, theestimated population size was 2,351 individuals in totalincluding 804 adults, excluding the few yews scatteredoutside this area. In 1925, there were c. 100 individualson the 2.18 ha east of the main trail through the plot(Helms, 1925). In 1998, the estimated population size inthis smaller area was 1839, including 655 adults. Astrongly expanding population is consistent with thepopulation structure at all three Munkebjerg plots(Fig. 2).

We estimated how many of the individuals alive in1998 that could have been present east of the main trailin 1925 given their diameter in 1998 and assuming var-ious growth rates. Using growth rates of 1.0, 2.0, 2.5,and 3.0 mm yrÿ1, 434, 186, 104, and 63 of the indivi-duals, respectively, could have been present in these 2.18ha in 1925. Helm's (1925) estimate of c. 100 yews isclosest to what we obtained using 2.5 mm yrÿ1, assum-ing zero mortality. This rate seems reasonable since thegrowth rates estimated from three large yews (Table 3)were in the range 1.4±2.6 mm yrÿ1, most yews in thepopulation were younger than these three, and growthrates decline with age (Lange, 1968). Even a growth rateas low as 1.0 mm yrÿ1 would have necessitated a strongpopulation increase of c. 320% over the 73 year periodas we estimate 1839 yews, including 655 adults, in the2.18 ha today. Using the 2.5 mm yrÿ1 rate, 169 indivi-duals would have been present in the whole 3.11 ha in1925.

The seedling and sapling to adult ratios were rela-tively low, but showed considerable heterogeneity indi-cating poorest recruitment on the sandy slope (Edgeplot; Table 2).

At Munkebjerg, the sex ratio of fertile individuals washighly skewed towards females (Table 4). In total, 139females and 66 males were encountered, a strong devia-tion from the expected 1:1 ratio (Gadj=26.522, df=1,p<0.001).

3.2. The importance of light availability for strobilusproduction and recruitment

The probability of sexual reproduction increasedstrongly with diameter and also with canopy openness(Fig. 3). Both relationships were highly signi®cant(Table 5). The sex of an individual was not related tosex or canopy openness (Table 5). Strobilus productionincreased strongly with diameter and also with canopyopenness (Fig. 4). Additionally, males produced morestrobili than females (Fig. 4). These relationships werehighly signi®cant (Table 5).

At Munkebjerg, the median understorey illuminationindex of seedlings, saplings, and adults were 2.0 (n=92),2.5 (n=148), and 3.0 (n=150), respectively. The under-storey illumination di�ered signi®cantly among thethree groups (Kruskal±Wallis one-way ANOVA,p<0.0001). Saplings occurred at microsites with ahigher understorey illumination score than seedlings(Wilcoxon's two-sample test, p=0.012). Only 31% ofthe seedlings occurred under an open canopy, while56% of the saplings did, a highly signi®cant di�erence(G=13.995, p<0.001).

At Marselisborg, the median understorey illumina-tion index of seedlings, saplings, and adults were 2.5(n=8), 2.5 (n=8), and 2.65 (n=4), respectively. Therewas no signi®cant di�erences among the three groups(Kruskal±Wallis one-way ANOVA, p>0.1). Using thebinary exposure index gave the same result: 63% ofseedlings (n=8), 63% of saplings (n=8), and 75% ofadults (n=4) occurred under an open canopy.

Thus, at Munkebjerg recruitment from the seedling tothe sapling stage occurred preferentially in microsites ofrelatively high light availability, while this cannot bedocumented from Marselisborg. The explanation forthis di�erence is that in Marselisborg Skov, seedlingsalready occurred at microsites of elevated light avail-ability (as compared to Munkebjerg).

Table 2

Area sampled, number of individuals (N), density, seedling/adult ratio (SE/A), and sapling/adult ratio (SA/A) of yews at the two study sites in 1998

Site Area N Density SE/A SA/A

haTotal Seedlings Saplings Adults

No.haÿ1 No.haÿ1 No.haÿ1 No.haÿ1

Munkebjerg

Core plot 0.16 222 1388 225 650 513 0.44 1.27

Edge plot 0.35 95 271 49 77 146 0.36 0.53

Bottom plot 0.10 73 730 400 170 160 2.50 1.06

Marselisborg 9.46 20 2.1 0.8 0.8 0.4 2.00 2.00

176 J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182

3.3. Spatial expansion

At Munkebjerg, two areas were source areas for yews:the main population and the Munkebjerg Hotel 100±200 m south of the main population. A number of adult

yews occurred at the hotel, some probably planted,others possibly self-seeded. Of the 6.0 km of trails thatwe censused, 1.6 km was within 200 m from at least oneof these two source areas, while 4.4 km was >200±800m away. Nine yews were encountered 4200 m awayfrom the source areas, while only four were encounteredfurther away. Thus, 4200 m from the source areas theyew density was 5.7 kmÿ1, while at distances >200 mthe density was only 0.9 km trailÿ1. This di�erence washighly signi®cantly di�erent from a random dispersion(Gadj=10.048, df=1, p<0.005).

In the 9.46 ha plot in Marselisborg Skov, we recorded20 individuals (Table 2). The average density of yewswas low compared to Munkebjerg, but the high seedling

Table 3

Long-term growth rates of some large yews from the Munkebjerg population

DBH

1998 (mm)

DBH

1925 (mm)

DBH

1872 a (mm)

Growth rate

1925±98 (mm yrÿ1)Minimumb growth rate

1872±1998 (mm yrÿ1)Maximum c growth rate

1872±1998 (mm yrÿ1)

Yew #429 301.6 133.6 4117.8 2.30 1.46 2.39

Yew #430 296.6 ÿ 4117.8 ÿ 1.42 2.35

Yew #75 325.8 ÿ 4117.8 ÿ 1.65 2.59

a Maximum DBH of the largest yews at the site in 1872 (Helms, 1925; Worsùe, 1985). The DBH of the three yews considered here might have

been smaller in 1872.bCalculated using 117.8 as the DBH in 1872.c Calculated using a zero DBH in 1872.

Table 4

Sex ratios in the Munkebjerg yew population

Site Female Male Ratio

Core plot 79 50 1.58

Edge plot 12 4 3.00

Bottom plot 40 9 4.44

Along trails 6 3 2.00

Fig. 2. Histograms showing the diameter distribution of yew Taxus baccata in Munkebjerg Strandskov (a±c) and Marselisborg Skov (d).

J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182 177

and sapling to adult ratios indicate an expandingpopulation (Table 2). The density was 6.8 yews haÿ1 atdistances 4100 m from the (northern) forest border,but an order of magnitude less, 0.8 yews haÿ1, at greaterdistances from the forest border. This di�erence washighly signi®cant (Gadj=10.972, df=1, p<0.001). AtMunkebjerg, the yew encountered furthest away fromthe hotel or the main population was 280 m away,while at Marselisborg the most distant yew was 315 maway from the nearest gardens. Additional explorationalong the trails in the rest of Marselisborg Skov did notreveal any yews more distant than this. As the Mun-kebjerg yew population has been formally protectedsince 1933 and informally protected in the precedingdecades, and gardens with yews have occurred for atleast 100 years in the surroundings of MarselisborgSkov, the rates of migration into these forests have beenabout 1±2 m yrÿ1 (maximum 3 m yrÿ1).

3.4. Forest management

The density of yew in Marselisborg Skov, only con-sidering areas 4100 m from the forest border, wasmuch higher in areas where the understorey was dense(12.5 yews haÿ1 in 1.12 ha) than in areas where theunderstorey was sparse (1.6 yews haÿ1 in 1.23 ha). Thisdi�erence was highly signi®cant (Gadj=20.719, df=1,p<0.001). In total, three of four adults, seven of eightsaplings, and six of eight seedlings stood in areas withdense understorey.

4. Discussion

4.1. Status of the Munkebjerg population

The yew population at Munkebjerg has increasedfrom <200 individuals in 1925 (Helms, 1925) to >2,000in 1998. The population structure at Munkebjerg, beinghighly skewed towards small individuals, was consistentwith an increasing population, and we observed abun-dant regeneration both by seeds and by layering and theproduction of multiple trunks around stem bases.

The female-biased sex ratio found in the Munkebjergpopulation could have arisen simply by chance when thepopulation size was small, later being conserved by clo-nal reproduction. A slight tendency for females toreproduce at an earlier stage than males (Fig. 4) mightalso be involved, but cannot explain the strong biasobserved. A female-biased sex ratio is not a generalphenomenon in yew, as the large population in theKingley Vale yew forest in England was male-biasedwith 286 males and 222 females recorded in four trans-ects (Gadj=8.092, df=1, p<0.005) (Williamson, 1978).

4.2. Importance of light availability

At Munkebjerg, sexual activity, strobilus production,and recruitment to the sapling stage were all reducedunder a dense canopy (Figs. 2±4). Thus, although yew isshade-tolerant (e.g., Brzeziecki and Kienast, 1994;Bugala, 1978; Ellenberg, 1988), it is favoured by an

Table 5

Logistic regression analysis of reproductive status and sex as a function of diameter and exposure and strobilus production as a function of diameter,

sex, and canopy openness

Dependent variable Explanatory variables Whole-model P Uncertainty coe�cient

Diameter Sex Canopy

Reproductive status **** ÿ ** **** 0.48

Sex ÿ ÿ ÿ ns ÿStrobilus production **** ** ** **** 0.16

The ®rst analysis include all Munkebjerg yews (n=405), while the second and third only include the fertile individuals (n=205). ns: p>0.10; (*);

p40.10; *: p40.05; **: p40.01; ***: p40.001; ****: p40.0001.

Fig. 3. Bar chart showing the percentage fertile individuals as a

function of diameter and canopy openness.

178 J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182

open canopy. This result is consistent with observationsof many other authors: yew has been reported not toproduce fruits under a closed beech canopy (Watt,1926), and in Taxus brevifolia Nutt. strobilus produc-tion was strongly enhanced under an open canopy(DiFazio et al., 1997). Czatoryski (1978a) states thatseedlings only survive and grow where the canopy isrelatively thin, and sapling recruitment has been asso-ciated with opening of the canopy (Hulme, 1996; Krol,1978). Likewise lack of recruitment has been attributedto heavy shade (Krol, 1978). It has been reported thatyew grows poorly under a closed beech canopy, butoptimally under an open canopy (Watt, 1926; Krol,1978), and diameter growth and branch productionwere also increased under an open canopy in Taxusbrevifolia (DiFazio et al., 1997). Finally, mortality ofeven large yews and the general decline of a Caucasianyew population has been suggested to be a result ofshading and other negative interactions with taller-sta-tured trees (Pridnya, 1984), and a Polish yew populationthat is rapidly declining due to lack of recruitment andmortality of adults grows under a dense canopy (Cza-toryski, 1978a). Conversely, yew has showed stronglocal expansion in Irish oak woods subsequent tocanopy openings (Mitchell, 1988, 1990b), and thestrongly expanding Munkebjerg population growsunder open canopy conditions.

We suggest that succession from the open degener-ated forests of the past towards denser forests, oftendominated by the highly shade-giving beech (e.g.,Ellenberg, 1988) is probably the cause of the poor statusof many declining yew populations. Until around 1800AD or even later most European forests were keptopen by grazing, coppicing etc., and succession towards

darker and more closed conditions has occurred whenthese uses were abandoned (e.g., Aaby, 1986; Andersen,1989; Andersson and Appelquist, 1990; Ellenberg, 1988;Fritzbùger, 1994; Jahn, 1991; Peterken, 1996).

The negative e�ect of a dense canopy on growth,survival, and reproduction in yew may explain char-acteristic patterns in the Quaternary history of yew inEurope. During the previous interglacials yew has beenable to achieve very high abundance in parts of tempe-rate Europe, commonly as short-term peaks during themesocratic phase, when yew expanded opportunisticallyas large-statured trees decreased in abundance, butquickly giving way to the same species again (Beug,1979; Erd, 1978; Nilsson, 1983; Nùrrevang and Lundù,1979). Opportunistic yew peaks also occurred duringthe Holocene, e.g. after the elm decline in Ireland(Mitchell, 1988, 1990a,b; O'Connell et al., 1987;PenÄ alba, 1994; Sarmaja-Korjonen et al., 1991; Watts,1985). Yew was also abundant in Ireland during thetelo-/oligocratic phase of the Gortian (Holsteinian)interglacial when large-statured trees, except Alnus werescarce due to poor soil conditions and a very oceanicclimate (Watts, 1967, 1985). Finally, yew has beenabundant on wet soils in England and northwesternGermany earlier in the Holocene, and was associatedwith wet soil conditions during the Eemian interglacialin Denmark (Andersen, 1975; Godwin, 1975; Wheeler,1992). As yew does not prefer wet soils per se and iseven susceptible to poor drainage (e.g., Ellenberg, 1988;Godwin, 1975; Krol, 1978; Williamson, 1978), we sug-gest that these associations arose because the forestcanopy on wet soils is dominated by less shade-givingspecies (e.g., Ellenberg, 1988), allowing a relativelyhigh understorey light availability. Thus, there is much

Fig. 4. Histogram showing the strobilus production (average number of strobili per ®rst-order shoot) as a function of diameter, sex, and canopy

openness (O=open canopy, D=dense canopy).

J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182 179

evidence for light availability having been a strong lim-iting factor for yew abundance and distribution duringbenign climatic periods throughout the Quaternary.

4.3. Factors involved in the present yew decline

Our results indicate that succession leading to dom-inance of tall-statured, shade-giving trees could beresponsible for the decline of many yew populations,but fail to support any of the other hypotheses for theyew decline. No rabbits occur at Munkebjerg, and theyews to do not show any signs of browsing by deer(pers. obs.), and did not do so in 1925 either (Helms,1925). Thus, herbivory by deer and rabbits was notimportant at Munkebjerg, but the importance of herbiv-ory has been documented at other sites where densities ofthese animals were very high (HñggstroÈ m, 1990; Kelly,1981; Mitchell, 1988, 1990a,b; Watt, 1926; Williamson,1978). No evidence for excessive seed or seedling pre-dation could be found, and seedlings did not show anypreference for especially protected microsites. Indeedvery few spiny shrubs were found within the mainpopulation. Likewise, no evidence for autotoxicity orsoil pathogens was found, and recruitment was commoneven close to large individuals (pers. obs.). Whetherchanging soil conditions could be responsible for thedecline of yew in other areas could not be evaluated, butwe do not believe that to be very likely given the widerange of edaphic conditions under which yew naturallyoccurs (e.g., Ellenberg, 1988; Godwin, 1975; Krol, 1978;Tittensor, 1980; Williamson, 1978). Thus, both lightavailability and herbivory can be important factors in¯u-encing the development of yew populations, while theimportance of the other factors still remains to be shown.

4.4. Recolonization by yew

The rates of 1±2 m yrÿ1 for the main yew invasionand 3 m yrÿ1 for the furthest individuals are similar tothe rates of migration into contiguous forest standsreported for the quickest spreading North Americanforest understorey species (Matlack, 1994). Seed dis-persal mode had a strong in¯uence on migration rates inthese species, endozoochory by birds or wide-rangingmammals providing the highest migration rates(Matlack, 1994). As the main seed dispersal mode ofyew is endozoochory by birds (Bartkowiak, 1978;Hulme, 1996; Milner, 1992), yew ®ts the pattern foundfor the North American species.

While the migration rate of yew is fast compared toother understorey species, it is still slow in absoluteterms, just a few hundred metres in a hundred years,and the population build-up is even slower, as evidencedby the low population density at Marselisborg and awayfrom the main population at Munkebjerg. Thus, if yewis to achieve a wider occurrence in the Danish woods

within the next century, reintroductions will be neces-sary. Otherwise, restocking will be slow and, except inthe neighbourhood of Munkebjerg, of garden origin.Reintroduction using seeds from the Munkebjergpopulation and possibly the closest populations outsideDenmark would be preferable. Reintroduction has alsobeen suggested as a conservation measure for yew inPoland (Czatoryski, 1978a), and has already been suc-cessfully implemented in several Polish forests (Krol,1978). Arti®cial reintroduction has also been mentionedas a way to overcome inadequate dispersal in Taxusbrevifolia (Busing et al., 1995).

4.5. Yew conservation and forest management

Regarding the Munkebjerg yew population, it isnotable that the canopy above much of the main popu-lation, particularly above the centre of the population,where yew densities were highest, was very open due tothe felling of many large beech trees. Selective cutting ofbeech trees has been practiced regularly since the areawas protected in 1933, and is also part of the Munici-pality of Vejle's future management plan for the area (S.Hedrup, pers. comm.). Taking the importance of lightavailability in yew population ecology into account, thismanagement is clearly to a large degree responsible forthe good status of the population. Thinning of the treestand has also been advocated for improving the statusof a Polish yew population (Czatoryski, 1978a), and hasalso already been practiced successfully, albeit unin-tentionally in an Irish oak wood, where yew expandedvery rapidly and strongly with the opening of thecanopy when most of the mature oak trees were felledabout 1800 AD (Mitchell, 1988).

Understorey clearance and the dense plantations ofexotic conifers, two phenomena that are common inDanish forestry, impede the re-establishment of yew inDanish forests. Understorey clearance had a negativee�ect on yew establishment at Marselisborg. At Mun-kebjerg no yews were found in the dark conifer planta-tions, albeit some of these occurred adjacent to the mainpopulation (pers. obs.). This is not surprising given thelight dependency of yew. The con¯ict between forestmanagement and the conservation of yew represents acommon problem in Danish nature conservancy, andthe intense management of Danish forests has beenidenti®ed as the most important threat towards rare,declining or threatened species in Denmark (Asbirk andSùgaard, 1991; Christensen and Emborg, 1996).

5. Conclusion

The yew population in Munkebjerg Strandskov washealthy and the management was satisfactory, but ifyew is to expand its range signi®cantly in Denmark

180 J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182

within a foreseeable future, reintroductions arerequired. The intense management of Danish forests,including much of the forest surrounding the Munkeb-jerg population, impedes the recolonization by yew.While yew is shade-tolerant, it is much favoured bybroken or thin canopy conditions, a factor that has hada strong impact on its abundance and habitat pre-ferences throughout the Quaternary. This is still true,where the two most important causes for the decliningstatus of many extant yew populations in Europe areprobably succession towards dense dark forests andintense herbivory by deer and rabbits where these ani-mals have dense populations.

Acknowledgements

Thanks to Steen Hedrup, nature guide at the Muni-cipality of Vejle for important information, FlemmingNùrgaard for making Fig. 1, and Rolf Svenning for helpwith the ®eld work. Also thanks to Jens Mogens Olesenand Axel D. Poulsen for their many useful comments.We are grateful to Mag.art. Marcus Lorenzens Legatand the Faculty of Natural Sciences, University of Aar-hus for economic support.

References

Aaby, B., 1986. Trees as anthropogenic indicators in regional pollen

diagrams from eastern Denmark. In: Behre, K.-E. (Ed.), Anthro-

pogenic indicators in pollen diagrams, A.A. Balkema, Rotterdam,

pp. 73±93.

Andersen, S.T., 1975. The Eemian freshwater deposit at Egernsund,

South Jylland, and the Eemian landscape development in Denmark.

Danmarks Geologiske Undersùgelser, AÊ rbog 1974, 49-70.

Andersen, S.T., 1989. Natural and cultural landscapes since the Ice

Age: shown by pollen analyses from small hollows in a forested area

in Denmark. J. of Danish Archaeology 8, 188±199.

Andersson, L., Appelquist, T., 1990. Istidens store vaÈ xtaÈ tare utfor-

made de nemorale och boreonemorale ekosystemen - en hypotes

med konsekvenser faÈ r naturvaÊ rden. Svensk Botanisk Tidskrift 8,

355±368.

Anonymous 1982. Danmark 1:100000 ± topogra®sk atlas. Geodñtisk

Institut, Copenhagen, Denmark.

Asbirk, S., Sùgaard, S., 1991. Rùdliste 90 ± sñrligt beskyttelseskrñ-

vende planter og dyr i Danmark. National Forest and Nature

Agency, Danish Ministry of Environment and Energy, Copenhagen,

Denmark.

Bartkowiak, S., 1978. Seed dispersal by birds. In The yew ± Taxus

baccata L. In: Bialobok, S. (Ed.) Foreign Scienti®c Publications

Department of the National Center for Scienti®c, Technical, and

Economic Information, (for the Department of Agriculture and the

National Science Foundation, Washington D.C.) Warsaw, Poland,

pp. 139±146.

Beug, H.-J., 1979. Vegetationsgeschichtlich-pollenanalytische Unter-

suchungen am Rix/WuÈ rm-Interglazial von Eurach am Starnberger

See/Obb. Geologica Bavaria 80, 91±106.

Broekmeyer, M.E.A., Vos, W., 1993. Forest reserves in Europe: a

review. In: Broekmeyer, M.E.A., Vos, W., Koop, H. (Eds.), European

Forest Reserves. Pudoc Scienti®c Publishers, Wageningen, pp. 9±28.

Brzeziecki, B., Kienast, F., 1994. Classifying the life-history strategies

of trees on the basis of the Grimean model. Forest Ecology and

Management 69, 167±187.

Bugala, W., 1978. Systematics and variability. In The yew - Taxus

baccata L. In: Bialobok, S. (Ed.), Foreign Scienti®c Publications

Department of the National Center for Scienti®c, Technical, and

Economic Information, (for the Department of Agriculture and the

National Science Foundation, Washington D.C.), Warsaw, Poland,

pp. 15±32.

Busing, R.T., Halpern, C.B., Spies, T.A., 1995. Ecology of Paci®c yew

(Taxus brevifolia) in Western Oregon and Washington. Conserva-

tion Biology 9, 1199±1207.

Christensen, M., Emborg, J., 1996. Biodiversity in natural versus

managed forest in Denmark. Forest Ecology and Management 85,

47±51.

Clark, D.A., Clark, D.B., 1992. Life history diversity of canopy and

emergent trees in a neotropical rain forest. Ecological Monographs

62, 315±344.

Clark, D.B., Clark, D.A., Rich, P.M., 1993. Comparative analysis of

microhabitat utilization by saplings of nine tree species in neo-

tropical rain forest. Biotropica 25, 397±407.

Czatoryski, A., 1978a. Protection and conservation of yew. In The

yewÐTaxus baccata L. In: Bialobok, S. (Ed.), Foreign Scienti®c

Publications Department of the National Center for Scienti®c,

Technical, and Economic Information (for the Department of

Agriculture and the National Science Foundation, Washington

D.C.), Warsaw, Poland, pp. 116±138.

Czatoryski, A., 1978b. Yew in the past. In The yewÐTaxus baccata

L. In: Bialobok S. (Ed.), Foreign Scienti®c Publications Depart-

ment of the National Center for Scienti®c, Technical, and Economic

Information, (for the Department of Agriculture and the National

Science Foundation, Washington D.C.), Warsaw, Poland, pp. 110±

115.

DiFazio, S.P., Vance, N.C., Wilson, M.V., 1997. Strobilus production

and growth of Paci®c yew under a range of overstory conditions in

western Oregon. Canadian Journal of Forest Research 27, 986±993.

Ellenberg, H., 1988. Vegetation Ecology of Central Europe. Cam-

bridge University Press, Cambridge.

Erd, K., 1978. Pollenstratigraphie im Gebiet der skandinavischen

Vereisungen. Schriftenreihe fuÈ r geologische Wissenschaften 9, 99±119.

Fritzbùger, B., (1994). Kulturskoven: Dansk skovbrug fra oldtid til

nutid. Gyldendal, Copenhagen, Denmark.

Gill, R. M. A., Gurnell, J., Trout, R. C., 1995. Do woodland mammals

threaten the development of new woods. In: Ferris-Kahn, R. (Ed.),

The ecology of woodland creation. Wiley, Chichester, pp. 201±224.

Godwin, H., 1975. The history of the British ¯ora. Cambridge: Cam-

bridge University Press.

Gravesen, P., 1986. Forelùbig oversigt over botaniske lokalitetet. 5.

Vejle Amt. The Danish Ministry of Environment, Copenhagen,

Denmark.

HñggstroÈ m, C.-A., 1990. The in¯uence of sheep and cattle grazing on

woodland meadows in AÊ land, SW Finland. Acta Botanica Fennica

141, 1-28.

Helms, J., 1925. Gamle taks i Danmark. Den Kongelige Veterinñr ±

og Landbohùjskole Aarskrift, 186-248.

Hulme, P.H., 1996. Natural regeneration of yew (Taxus baccata L.):

microsite, seed or hebivore limitation? J. of Ecology 84, 853±861.

Jahn, G., 1991. Temperate deciduous forests of Europe. In: RoÈ hrig,

E., Ulrich, B. (Eds.), Temperate deciduous forests, vol. 7. Elsevier,

Amsterdam, pp. 377±502.

Kelly, D.L., 1981. The native forest vegetation of Killarney, south-

west Ireland: an ecological account. J. of Ecology 69, 437±472.

Kral, R., 1983. A report on some rare, threatened, or endagered for-

est-related vascular plants of the South. Isoetaceae through

Euphorbiaceae, vol. 1. USDA Forest Service, Atlanta, Georgia.

Krol, S., 1978. An outline of ecology. In The yewÐTaxus baccata L.

In: S. Bialobok (Ed.), Foreign Scienti®c Publications Department of

J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182 181

the National Center for Scienti®c, Technical, and Economic

Information, (for the Department of Agriculture and the National

Science Foundation, Washington D.C.), Warsaw, Poland, pp. 65±

86.

Lange, J., 1968. Bromùletaksens alder. Dansk Dendrologisk AÊ rsskrift,

73±79.

Lewandowski, A., Burczyk, J., Mejnartowicz, L., 1995. Genetic struc-

ture of English yew (Taxus baccata L.) in the Wierzchlas Reserve:

implications for genetic conservation. Forest Ecology and Manage-

ment 73, 221±227.

Matlack, G.R., 1994. Plant species migration in a mixed-history forest

landscape in eastern North America. Ecology 75, 1491±1502.

Milner, J.E., 1992. The Tree Book. Collins and Brown, London.

Mitchell, F.J.G., 1988. The vegetational history of the Killarney oak-

woods, SW Ireland: evidence from ®ne spatial resolution pollen

analysis. J. of Ecology 76, 415±436.

Mitchell, F.J.G., 1990. The history and vegetation dynamics of a yew

wood (Taxus baccata L.) in S.W. Ireland. New Phytologist 115,

573±577.

Mitchell, F.J.G., 1990. The impact of grazing and human disturbance

on the dynamics of woodland in S.W. Ireland. J. of Vegetation Sci-

ence 1, 245±254.

Mùller, P.F., Staun, H., 1995. Danmarks Skove. Politikens Forlag,

Copenhagen.

Moore, P.D., 1996. Hunting ground for farmers. Nature 382, 675±676.

Nemecek, S., 1996. Rescuing an endagered tree. Scienti®c American,

p. 10.

Nilsson, T., 1983. The Pleistocene: geology and life in the quaternary

ice age. Reidel Publishing Company, Dordrecht.

Nùrrevang, A., Lundù, J., 1979. Danmarks natur 1: Landskabernes

opstêen, 2nd ed. Politekens Forlag, Copenhagen.

Nùrrevang, A., Lundù, J., 1980. Danmarks natur 6: Skovene. Politi-

kens Forlag, Copenhagen.

Nùrrevang, A., Lundù, J., 1981. Danmarks natur 9: Det bebyggede

land. Politikens Forlag, Copenhagen, Denmark.

O'Connell, M., Mitchell, F.J.G., Readman, P.W., Doherty, T.J.,

Murray, D.A., 1987. Palaeoecological investigations towards the

reconstruction of the post-glacial environment at Lough Doo,

County Mayo, Ireland. J. of Quaternary Science 2, 149±164.

PenÄ alba, M.C., 1994. The history of the Holocene vegetation in

northern Spain from pollen analysis. J. of Ecology 82, 815±832.

Peterken, G.F., 1996. Natural woodland: ecology and conservation in

northern temperate regions. Cambridge University Press, Cambridge.

Pridnya, M.V., 1984. Phytocenotic status and structure of the Khosta

common-yew population in the Caucasus Biosphere Reserve. Soviet

J. of Ecology 15, 1±6.

Sarmaja-Korjonen, K., Vasari, Y., HñggstroÈ m, C.-A., 1991. Taxus

baccata and in¯uence of Iron Age man on the vegetation in land

S.W. Finland. Acta Botanica Fennici 28, 143±159.

Sokal, R.R., Rohlf, F.J., 1995. Biometry: the principles and practice of

statistics in biological research, 3rd ed. Freeman, New York.

Stace, C., 1997. New ¯ora of the British Isles, 2nd ed. Cambridge

University Press, Cambridge.

Suszka, B., 1978. Generative and vegetative reproduction. The yewÐ

Taxus baccata L. In: Bialobok S. (Ed.), Foreign Scienti®c Publica-

tions Department of the National Center for Scienti®c, Technical,

and Economic Information (for the Department of Agriculture and

the National Science Foundation, Washington D.C.), Warsaw,

Poland, pp. 87±102.

Tittensor, R.M., 1980. Ecological history of yew Taxus baccata L. in

southern England. Biological Conservation 17, 243±265.

Tutin, T.G., 1953. The vegetation of the Azores. J. of Ecology 41, 53±61.

Tutin, T.G., Heywood, V.H., Burges, N.A., Valentine, D.H., Walters,

S.M., Webb, D.A., 1964. Flora europaea. Lycopodiaceae to Plata-

naceae, vol. 1. Cambridge University Press, Cambridge.

Watt, A.S., 1926. Yew communities of the South Downs. J. of Ecology

14, 282±316.

Watts, W.A., 1967. Interglacial deposits in Kildromin Townland, near

Herbertstown, Co. Limerick. Proceedings of the Royal Irish Acad-

emy sect. B 65, 339±348.

Watts, W.A., 1985. Quaternary vegetation cycles. In: Edwards, K.J.,

Warren, W.P. (Eds.), The Quaternary history of Ireland. Academic

Press, London.

Watts, W.A., Allen, J.R.M., Huntley, B., Fritz, S.C., 1996. Vegetation

history and climate of the last 15,000 years at Laghi di Monticchio,

southern Italy. Quaternary Science Reviews 15, 113±132.

Wheeler, A.J., 1992. Vegetational succession, acidi®cation and allo-

genic events as recorded in Flandrian peat deposits from an isolated

Fenland embayment. New Phytologist 122, 745±756.

Williamson, R., 1978. The Great Yew Forest. MacMillan, London.

Worsùe, E., 1985. Er taks (Taxus baccata L.) vildtvoksende i Dan-

mark? Flora og Fauna 91, 22±26.

182 J.-C. Svenning, E. MagaÊrd/Biological Conservation 88 (1999) 173±182