Temporal changes (1986–1999) in populations of primrose(Primula vulgaris Huds.) in an agricultural landscape and

implications for conservation

Patrick Endelsa,*, Hans Jacquemyna,*, Rein Brysb, Martin Hermya,*, Geert De Blustb

aLaboratory for Forest, Nature and Landscape Research, Catholic University of Leuven, Vital Decosterstraat 102, B-3000 Leuven, BelgiumbInstitute of Nature Conservation, Kliniekstraat 25, B-1070 Brussels, Belgium

Received 13 November 2000; received in revised form 20 June 2001; accepted 22 June 2001

Abstract

In Belgium, Primula vulgaris is a rare and declining species. Its fate is bound up with the ever-changing agricultural landscape in

northwestern Belgium and analysis of historical data showed a shrinking distribution area during the last decades. Contrary to thesituation in England and France, most of the populations are situated in small landscape elements in the agricultural landscape andnot in woodland. The population size distribution is skewed to very small populations (<10 individuals) with few younger life

stages in small populations, higher proportions of older adults and unequal flower morph numbers. The changes in several popu-lation traits during a 13-year interval are correlated with initial population status, indicating that small populations tend to be moreprone to extinction than larger ones. Small remnant woodland patches may be seen as ‘safe sites’: in this environment population

sizes were more or less stable during the 13-year period whereas populations in ditches around arable fields were particularly sus-ceptible to decline. Under current conditions, the long term survival of the species in small landscape elements is highly criticalunless land use practices change drastically in the near future. The minimum viable populations concept and management of smalllandscape elements are discussed. # 2002 Elsevier Science Ltd. All rights reserved.

Keywords: Primula vulgaris; Rare plant species distribution; Minimum viable populations; Small landscape elements; Time series

1. Introduction

Small landscape elements are believed to function asnatural corridors between habitat patches in fragmentedlandscapes, but the extent to which they really act ascorridors is still a subject of debate (Burel and Baudry,1990; Forman, 1991; Fritz and Merriam, 1993; Corbit etal., 1999). However, ditches, hedgerows and other smalllandscape elements do function as important habitatrefuges for the survival of many plant species fromwoodlands (e.g. Pollard, 1973; Peterken and Game,1981; Middleton and Merriam, 1983; Corbit et al., 1999;Honnay et al., 1999). Since habitat fragmentation anddeterioration force an increasing number of plant spe-cies to survive in remnant (semi-)natural structures in

the agricultural landscape, their importance is expectedto increase.

Although once widespread in many parts of WesternEurope, small landscape elements, in particular hedge-rows and trees, have decreased dramatically due to thenegative effects of intensive agriculture, spreading(sub)urbanisation and a continuous improvement andincrease in infrastructure (Poiret, 1999; Baudry et al.,2000b). As a result, the traditional small-scaled land-scape consisting of a dense network of hedgerows, dit-ches and rows of trees is subjected to radical changesand is likely to disappear in the long term and with thema considerable number of species that occur in theselandscape elements. For example, Bunce et al. (1994),showed there was a 24% loss of hedgerows from 1978 to1990 in the Great Britain countryside and an associateddecline of species richness, mainly in pastural land-scapes.

Besides decreasing in area, the remnant elements arealso subjected to changes in management and nutrient

0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.

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Biological Conservation 105 (2002) 11–25

www.elsevier.com/locate/biocon

* Corresponding author. Tel.: +32-1632-9769; fax: +32-1632-

9760.

E-mail address: patrick.endels@agr.kleuven.ac.be (P. Endels).

or moisture conditions, which may have an importantimpact on vegetation structure and composition. Nutri-ent enrichment from adjacent fields is likely to result ina decrease of species diversity (Kleijn and Verbeek,2000) mainly as a consequence of changing competitiveinteractions between plant species (cf. Grime, 1979; Til-man, 1982, 1988; Berendse, 1994; Bobbink et al., 1998),while increased drainage may also have pronouncednegative effects on species richness too. In addition, themanagement has often changed radically: grass vergesalong farm fields were previously mown and hedgerowswere neatly trimmed, but now these practices have beenabandoned and are often replaced by herbicide applica-tion and clearing of hedgerows (Baudry et al., 2000b).Management is highly dynamic and may change fromyear to year in relation to agro-economic demands. Ingeneral it can be expected that species most vulnerableto these changes are those that occur at low within-population densities.

Given the current pressure, one might ask whethertraditional small landscape elements will in the longterm effectiviely act as habitat refuges for plant species.There are only a few studies that have investigated plantpopulation persistence in small landscape elements (e.g.Fritz and Merriam, 1993). This information, however, isimportant if we are to predict the survival of many plantspecies in our modern, cultural landscapes. Therefore, adeeper insight into the main factors affecting the num-ber of individuals of a species within small landscapeelements is needed. Following Schemske et al. (1994),assessment of the biological status of the species is thefirst important step to determine survival probability.Trends in distribution patterns, population size andstructure may be the first indicators for the way speciesrespond to changing environmental conditions and mayform the basis for more detailed demographic andgenetic monitoring. Only when the biological status ofthe species is known, it is it possible to initiate effectiverecovery efforts to ensure the long term survival of thespecies (Schemske et al., 1994).

We studied the distribution of primrose (Primula vul-garis), a rare and declining woodland species of whichthe distribution in Belgium is limited almost exclusivelyto small landscape elements. As such this species pro-vides great opportunities to study population persis-tence in small landscape elements embedded in a hostileagricultural matrix. Moreover, the results of this studymay contribute to the conservation of many other plantspecies that occur in similar habitats. Past and presentstatus of the distribution at several scales are startingpoints for a more detailed analysis of changes inindividual populations over a 13-year period. Thesedistribution patterns and long term dynamics are linkedto habitat characteristics and population traits ofthe complete set of primrose populations in Belgium.The results of population surveys of this kind may

generate guidelines for land use planning and the devel-opment of management measures.

2. Methods

2.1. The species

P. vulgaris is a perennial herb characteristic of moist,shaded habitats, with a North Atlantic and Mediterra-nean distribution (Walter, 1970; Hegi, 1975; Hulten andFries, 1986, etc.). The populations in Northern Belgium(Flanders) are more than 40 km distant from largepopulations in France (Foret de Clairmarais-Rihoult;Gehu and Gehu-Franck, 1957). North of Belgium, thespecies is indigenous in brook valleys in the Drentheand Kempen district (Mennema et al., 1985). Elsewhere inThe Netherlands, P. vulgaris is most probably introducedas it is associated with old parks and castle gardens. Thespecies is apparently favoured by mild winter conditions(Gehu and Gehu-Franck, 1957). Its distribution, how-ever, does appear to be associated to some extent withsoil moisture and atmospheric humidity (Valentine,1948).

Flowers appear in early spring (March–April); theyare pale yellow, borne on separate stalks and are dysty-lous, restricting legitimate pollination to that betweenpin and thrum morphs. However, under certain cir-cumstances various rates of self-fertilisation may occur(Woodell, 1960; Ornduff, 1979; Bodmer, 1984). Seeddispersal occurs when capsules ripen around the middleof June. The seeds have an elaiosome which is attractiveto ants and small mammals, which may actively harvestseeds and in that way act as dispersers (Richards, 1984;Valverde and Silvertown, 1995). Bending of the flower-ing stalks towards the ground can be seen as an adap-tation to myrmecochory. Vegetative spread occurs onlywithin very short distances through the production oflateral rosettes.

2.2. Study area

The study area is located in the vicinity of Bruges andis south of the border region between the polder land-scape and a more sandy region (Fig. 1). This regioncorresponds with the historical distribution area ofP. vulgaris in Belgium (Vande Vyvere, 1958). Soils rangefrom coarse sand to fine sandy loam. Owing to a highdisturbance rate of the field margins and ditch bankhabitats, there is also a high variation in other soilcharacteristics: (pH ranges form 3.9 to 7.8 (n=67) andnutrient levels (N, P, K) are also highly variablebetween and within sites. The area is under intensiveagricultural use with increasing conversion of perma-nent pastures to fields of maize and a few other crops(potatoes, vegetables). Overall field size is also increasing,

12 P. Endels et al. / Biological Conservation 105 (2002) 11–25

damaging the ecological network mainly consisting oflines of trees, hedgerows, ditches and small forest pat-ches. Furthermore there is increasing urbanisation inrecent decades around the city of Bruges.

2.3. Data recording

To study temporal changes in primrose we workedwith two types of historical data. First, data on theoccurrence of primrose in Belgium for recent decadeswere gathered. Information on the presence of the spe-cies in a 1 km2 and 16 km2 square grid in Belgiumaccording to the IFBL (Institute for Floristics in Bel-gium and Luxemburg) survey system is available for thefollowing years: 1958 (Vande Vyvere, 1958), 1979 (VanRompaey and Delvosalle, 1979), and 1986 (M. Hermy,unpublished data). The latter dataset also includedobservations on the population size and structure for 34populations which allowed us to work on a moredetailed scale.

Based on the results of these earlier surveys and datafrom local nature conservation organizations, all thepotential habitats for P. vulgaris (ditch banks, forestedges, hedgerows and small furrows in deciduous forestpatches) within the study area were surveyed in earlyspring of 1999 for the presence of the species. Theexact location of all the populations was measuredwith GPS and all individuals were counted. A dis-tinction was made between seedlings, juveniles andadults (see below). Adults were categorized as pins,

thrums or non-flowering individuals, and the number ofrosettes was recorded. Apart from the number ofrosettes, similar data were obtained from for the 1986survey for a subset of populations (n=34); seedlingsnumbers were only recorded in 28 populations. Finally,observations were made on several habitat character-istics: habitat type, surrounding land use (forest, pas-tures or arable fields), exposure and inclination of thesite. Habitat characteristics were attributed according tothe main location of the plants within a population:sites with ditches bounded by permanent grassland onone side and arable land at the other, were classified asgrassland when most individuals were found on theditch bank adjacent to the pasture.

2.4. Determination of the different age categories

Since the actual age of individual plants of P. vulgariscannot be determined, the population structure analysiswas based on the number of individuals in the differentlife stages of the plant. These stages roughly relate toage (sensu Oostermeijer et al., 1994):

. seedlings: individuals developed directly after thegermination of seeds, with cotyledons still presentand often also one ‘normal’ leaf-pair.

. juveniles: (immature) plants without cotyledonsand with only one rosette of leaves. Juveniles canonly be distinguished from vegetative adults withone rosette by means of their size: an individual is

Fig. 1. Distribution of P. vulgaris in Belgium: results of the 1999 survey with location of the different populations and distances between central

points of the different population clusters (letters A–G).

P. Endels et al. / Biological Conservation 105 (2002) 11–25 13

considered as an adult when its leaf size is com-parable to flowering adults in the same population(since leaf size is clearly associated with vegetationstructure), if leaf size is significantly smaller thenthe individual is assigned to the juvenile category.

. vegetative adults: non-flowering individuals with-out cotyledons, with one or more rosettes, oftenshowing signs of overwintering leaves. Leaf size iscomparable to generative adults which are grow-ing under similar conditions.

. generative adults: plants baring one or more flow-ering stalks, having one or more rossettes andoften showing signs of older, overwintering leaves.

2.5. Data analysis

First, we investigated the temporal changes in thedistribution of primrose. To obtain a general over-view, the time series concerning the presence of thespecies in 1 km2 and 16 km2 square grids in Belgium(IFBL survey system) were mapped in a GIS (Geo-graphic Information System, Arcview 3.2, ESRI 1998).For each survey period, grid cells with presence of P.vulgaris were counted and compared with the distribu-tion in 1999.

We then focused on the current status of individualpopulations and temporal changes in population traits.Based on the raw data, we calculated several populationstructure measures: proportions of the different lifestages, difference between numbers of pin and thrumplants, effective population size (flowering adults) andmean number of rosettes per adult. These data werecalculated for both the 1999 and 1986 survey. We alsodetermined differences in life stage numbers between thetwo survey periods.

For the 1999 data, the populations were divided intothree groups according to their size and for these groupsproportions of the different life stages (seedlings, juve-niles and adults) were compared by Kruskal–Wallistests (Siegel and Castellan, 1988). The average numberof rosettes and differences in flower morphs were plottedagainst population size. Circular uniformity of siteaspect was tested by a Raleigh’s test (Zar, 1984). For thisprocedure, populations on flat surfaces were omitted.

Wilcoxon signed rank tests (Siegel and Castellan,1988) were performed to test for differences in popula-tion size and numbers per life stage between the 1999and 1986 survey. Given the assumption that—for sev-eral demographical and genetical reasons—the persis-tence of a population cannot be guaranteed when itssize is lower than a certain threshold (a minimum viablepopulation size; Shaffer, 1981; Ouborg, 1988; Boyce,1992), one may expect population dynamics to be cor-related with its initial population size. We thereforecalculated Spearman correlation coefficients between

the population size in 1986 and the changes in severalpopulation traits between the two survey periods, andcompared initial sizes of populations that disappearedduring the 13-year interval and populations that sur-vived. Survival probabilities were predicted with logisticregression and plotted against population size. Finally,we tried to explain population dynamics on the basis ofa number of contrasting habitat characteristics byapplying Mann–Whitney tests (Siegel and Castellan,1988). All statistical analyses were performed in SPSSversion 10.0.

3. Results

3.1. Overall development of the distribution area ofP. vulgaris in Belgium

The 1999 population distribution survey yielded anoverview of the species’ presence in the sandy region innorthern Belgium (Fig. 1). Its occurrence is limited totwo areas A and B with a relatively high populationdensity east of Bruges, plus two smaller areas there (Cand D), two others to the south of Bruges (E and G),and one near Diksmuide (F). Locations A and B arepart of a largely traditional agricultural landscapearound Sijsele–Oedelem–Donk. The distances betweenthese areas (Fig. 1) far exceed the natural dispersal dis-tance of the species. Within each area the shortest dis-tance between populations ranges from 7 m to 1956 m.

The three surveys between 1958 and 1999 show thatmost of the decline occurred before 1986 (Fig. 2) andwas particularly marked in the central part of the dis-tribution area. It was equally evident whether plotted ona 1 km2 or 16 km2 grid scale (Fig. 3).

3.2. Habitat characteristics

In our 1999 survey, 15% of the populations were insmall woodlands while 85% occurred on ditch sides atforest edges or in agricultural landscapes. Most hadsome shade from a single line of trees or from the steepslopes along ditches: for three out of five sites the slopewas >30% (Fig. 4c). The species did not show a pref-erence for a specific aspect (Raleigh’s test for circularuniformity, R=2.83, n=64, P>0.05), nor could a linkbetween aspect and slope be detected (Fig. 5).

3.3. Current status: population size and structure

Our 1999 survey revealed 89 populations whose sizeranged from 1 to 1219 individuals (mean=95, med-ian=20) (Fig. 6). Sixty-five percent of the populations(n=58) contained <50 plants. The larger populations(>500 individuals) constituted only 1% (n=4) of thetotal number. The numbers for the different life stages

14 P. Endels et al. / Biological Conservation 105 (2002) 11–25

also vary varied considerably from site to site. The dis-tribution of the number of seedlings and juveniles waseven more skewed than for adults (Fig. 7), indicatingthat most populations had few or no seedlings or juve-niles (10 individuals or less for 83% and 70% of thesites, respectively). Moreover, the proportion of seed-lings within a population was lower in small popula-tions (Fig. 8a, Kruskal–Wallis �2=29.0, P<0.001); the

opposite was found for the proportion of adults (Fig. 8b,Kruskal–Wallis �2=24.4, P<0.001). The trend towardsvery high proportions of older individuals withdecreasing population size is also suggested by the sig-nificantly higher mean number of rosettes per adult(Fig. 9) in small populations. Another important indi-cation for a disturbed population structure may be thepin–thrum ratio: while equal numbers of these two

Fig. 2. Retraction of range of P. vulgaris on a 1 km2 grid in Belgium. Open squares are those only occupied in 1958 (data form Vande Vyvere, 1958),

shaded squares are still or only occupied in 1986 (from Hermy, unpublished), and solid squares show grid cells still occupied in the 1999 survey.

Fig. 3. Numbers of (a) 1 km2 and (b) 16 km2 grid cells with the presence of P. vugaris in Belgium.

P. Endels et al. / Biological Conservation 105 (2002) 11–25 15

morphs were observed in larger populations (>100plants), there were many examples of small populationscontaining only one morph (Fig. 10).

3.4. Changes in population size and composition between1986 and 1999

3.4.1. Development of population sizes and compositionAnalysis of changes in the subset of 34 populations

monitored in 1986 and 1999 indicated a clear trendtowards increasing numbers of small populations(Fig. 11). During this 13 year period, the proportionwith <10 individuals increased from 26% to 41% whilethe proportion with >100 individuals declined from 24%to 18%. The fate of individual populations is shown inFig. 12: 24 of the 34 surveyed populations (71%)decreased in size between 1986 and 1999 and eightpopulations (24%) became extinct. A Wilcoxon signedranks test indicated that median population size andnumber of adults per population declined significantlyfrom 1986 to 1999 (Table 1). For the younger life stages,no significant differences were found. There was a clear

relationship between the fate of primrose populationsand the initial population size (Table 2). Indeed, acomparison of eight populations that became extinctwith 26 populations that survived the 13 year intervalshowed a significant difference in size in 1986 (medianpopulation 18 versus 59, respectively, Mann–WhitneyZ=2.32, P<0.05). This conclusion was supported bythe logistic regression analysis between extincton andpopulation size (model �2=6.22, n=34, P<0.05)(Fig. 13).

A comparison of this dataset with that for all 89populations recorded during the 1999 survey (Fig. 6)showed no significant difference in population size dis-tribution (Kolmogorov–Smirnov one-sample test,D=0.048, n=34, P>0.05). We may therefore extra-polate these conclusions about increasing numbers ofsmall populations, decreasing numbers of adults andrisk of extinction to the larger dataset.

3.4.2. Impact of habitat characteristics and land useChanges in the number of individuals per population

were related to habitat type and surrounding land use.The decline in overall population size in woodlands wasnot significant, whereas a much larger and significantdecline in non-woodland populations could be detected(Table 3). Similarly, there was no significant differencein population size between the two survey periods forthe populations surrounded by pastures or forests, but alarge and significant decline was found for those next tofields (Table 3).

Fig. 4. Number of populations of P. vulgaris for the different site

characteristics (n=89): (a) habitat type (1, furrows in woodland; 2,

ditches along forest edges; 3, ditches along a line of trees; 4, ditches

without shade; (b) surrounding land use (1, woodland; 2, pasture; 3,

arable fields; (c) inclination (0, no slope; 1, slight slope (0–30%); 3,

strong slope (>60%).

Table 1

Wilcoxon signed ranks tests for the difference in population size and

numbers of the different life stages for 34 populations of P. vulgaris

surveyed in 1986 and 1999

Median n Z

1986 1999

Total population size 38.5 18.5 34 2.35*

Number of adults 36 13 34 2.50*

Number of juveniles 2.5 2 34 0.62

Number of seedlings 0 0 28 1.54

* P<0.05.

Table 2

Spearman’s rank correlation coefficient (rs) between initial population

size recorded in 1986 and subsequent decline (expressed as the number

of individuals) between 1986 and 1999, for various life stages in 34

populations of P. vulgaris

Decline 1986–1999

Population Adults Juveniles Seedlings

Population size in 1986 rs �0.55** �0.53** �0.42* �0.35

n 34 34 34 28

* P<0.05.

** P<0.01.

16 P. Endels et al. / Biological Conservation 105 (2002) 11–25

4. Discussion

4.1. Habitat requirements

In England, primrose mainly occurs in woodlandwhere it is often associated with newly opened gaps(Whale, 1984; Valverde and Silvertown, 1995), althoughit can also be found in hedges and old grassland with

some protection from drought (Rackham, 1980). As oneproceeds west in the UK, the species becomes less tiedto woodland habitats (B. Davis, pers. comm.). A similargradient can be found on the Continent: while, aroundBruges (Fig. 1), primrose is mainly confined to ditchbanks along hedgerows and forest edges, populations inthe most western part of Flanders and Northern Franceare principally found in forests. The species’ presence in

Fig. 5. Polar scatterplot of aspect and slope for 64 sites (populations on flat surface were omitted) with P. vulgaris populations in Belgium. [ordinal

scale for the slope variable: 1, slight slope (0–30%); 2, average slope (30–60%); 3, strong slope (>60%)].

Table 3

Wilcoxon signed ranks tests for changes in population size between 1986 and 1999 in contrasting habitat and land use types for 34 populations of P.

vulgaris

n Median 1986 Median 1999 Z

Habitat type Furrows in woodland 18 36 18.5 1.46

Other 16 67 15.5 2.02*

Adjacent land use Arable field 10 58 8.5 2.19*

Pasture or forest 24 38.5 21.5 1.43

* P<0.05.

P. Endels et al. / Biological Conservation 105 (2002) 11–25 17

small elements in the agricultural landscape may bestriking, but to us this is no surprise, given the basichabitat requirements: although in Great Britain P. vul-garis performs best (highest biomass, flower production

and seed set) under a moderate amount of shade(Helliwell, 1980), its presence in woodland or forestedges in Great Britain is considered mainly a questionof shelter against from lower temperatures (Valentine,

Fig. 6. Population size distribution of P. vulgaris in 1999.

Fig. 7. Frequencies and descriptive statistics for the different life-stages (adults, juveniles and seedlings) for 89 populations of P. vulgaris in 1999.

18 P. Endels et al. / Biological Conservation 105 (2002) 11–25

1948) and drought (Whale, 1983, 1984). As primroseoften occurs along ditches (Fig. 4a), is of small statureand usually occurs in dense vegetation, it occupies amore or less protected micro-environment.

4.2. Changes in distribution and population traits

Our results clearly show that both the distribution ofP. vulgaris (Figs. 2 and 3) and population size (Fig. 11,Table 1) have changed drastically during the last 13years. A highly dynamic and intensive agriculture withthe accompanying removal of small landscape elementshas resulted in the extinction of eight populations withinthis period. Most other populations have decreased inpopulation size, making them more vulnerable to theeffects of stochasticity (see below). Analysis of popu-lation structure development may be less accurate forthe younger life stages, since these are more easilyoverlooked when counting individuals. Furthermore,seedling emergence may also vary considerably fromyear to year. However, there is an overall and unde-niable relationship between population size andstructure.

Minimum viable populations sizes (MVPs) varystrongly among species (Brauer et al., 1999) and a widerange of definitions is given (e.g. Franklin, 1980; Shaf-fer, 1981; Ouborg, 1988; Boyce, 1992). If we considerthe MVP to be the population size required for 90%probability of survival (cf. Brauer et al., 1999) between1986 and 1999, then it is clear that relatively few (n=20;22%) populations are above that size (95 individuals;Fig. 13). This means that the status of this species iscritical in terms of its long term survival. Given its lim-ited area of occupancy in Belgium (Fig. 2) and theobserved decline in number of locations, number ofmature individuals and area of occupancy (from 42 km2

in 1958 to 21 km2 in 1999; Fig. 2), the species should beclassified as endangered, according to the criteria forthreatened species categories endorsed by the IUCN(Mace and Lande, 1991; Keith, 1998). Since 1976, it ison the list of those species whose underground parts areprotected in Belgium, but flowers may be picked. Inpractice, there is no control and violations are rarelyprosecuted.

Thus, our results pose serious doubts on the viabilityof many plant species in small landscape elements inagricultural landscapes (cf. Bunce et al., 1994). Fieldobservations in the same region suggests a similar pro-blematic situation for species of semi-natural grasslands(e.g. Cardamine pratensis, Lychnis flos-cuculi, Luzulacampestris, Anthoxanthum odoratum, Serratula tinctoria)and woodlands (e.g. Anemone nemorosa, Viola riviniana,Polygonatum multiflorum). Zwaenepoel (1993), studyingverges of roads and rides in the agricultural landscape,assigned these species to a new ecological species groupof so-called ‘fence species’. Given our results, we have

little faith in ecological networks of small landscapeelements acting as stable refuges under the prevailingconditions and with current agricultural practices (cf.Poschold and Bonn, 1998), let alone that this networkfunctions as corridors for plant species (see also Corbitet al., 1999; Baudry et al., 2000a). The overall decline inpopulation sizes has to be attributed to a decline inhabitat quality (due to fertilisation, spraying, abandon-ment of field margin management), which is not expec-ted to ameliorate unless land use practices changedramatically (see below).

4.3. Viability of small populations of primrose

Although individual rosettes can die off each year,individual plants are relatively long-lived (10–30 years;Boyd et al., 1990) and one may expect that, once estab-lished, the species is not likely to disappear immediatelywhen the prevailing conditions no longer correspondwith the species’ requirements. Fischer and Stocklin

Fig. 8. Proportions of seedlings (a) and adults (b) in small, medium

and large populations of P. vulgaris in 1999.

P. Endels et al. / Biological Conservation 105 (2002) 11–25 19

(1997) demonstrated local extinction risks to be lowerfor species with longer life cycles. However, theobserved structure of the smaller populations (Figs. 8–10) suggests that they may represent non-viable relictswith low seedling and juvenile proportions, and unequalnumbers of flower morphs. Moreover, the fundamentalidea behind the minimum viable populations concept

(Shaffer, 1981; Soule, 1987)—the fact that small popu-lations are more likely to go extinct than larger ones—isclearly illustrated by the results of the two-period survey(Fig. 12, Table 2). The higher mean number of rosettesper plant in small populations may be the result of dif-ferent survival rates of individuals when site conditionsare deteriorating: bigger, more robust individuals are

Fig. 9. Relationship between mean number of rosettes per adult and population size (n=89) in 1999.

Fig. 10. Relationship between population size and the difference in numbers of thrum (T) and pin (P) plants for P. vulgaris populations (n=89) in

1999.

20 P. Endels et al. / Biological Conservation 105 (2002) 11–25

Fig. 11. Frequency of population sizes for 34 populations of P. vulgaris for the two survey periods (1986 and 1999).

Fig. 12. Changes in population sizes for 34 population of P. vulgaris. Records above the line of ‘no change’’ (x=y) represent sites with increased

population sizes (+); for records under this axis population sizes are lower in 1999 compared to 1986 (�).

P. Endels et al. / Biological Conservation 105 (2002) 11–25 21

likely to withstand longer the competition from sur-rounding vegetation or the negative impact of herbicidedrift. Marrs et al. (1993) have recorded high seedlingsensitivity to glyphosate spray drift for Lychnis flos-cuculi. In this case, field observations suggest thatdeterministic factors (systematic pressures, sensu Shaf-fer, 1981) such as habitat loss (due to parcel enlarge-ment) and human-induced habitat deterioration, as aresult of herbicide application, fertilizer runoff or aban-donment of mowing, may be the first step in populationdecline, causing reduced germination or seedlingrecruitment. It is very likely that these processes do notactually cause population extinction but they obviouslyaffect population size and composition (cf. Table 3).

With decreasing population size, the significance ofstochastic processes (inadequate mechanical cleaning ofditches, picking of flowers and/or collecting wholeplants) for the dynamics and genetic composition of apopulation is assumed to increase (Pimm et al., 1988;Menges, 1990; Menges, 2000; Oostermeijer et al., 1993).Recent studies (e.g. Fischer and Matthies, 1998a, b; Fischeret al., 2000; Kery et al., 2000) suggest that reduced plantperformance in small plant populations might havegenetic causes. Preliminary research into the genetics ofprimrose in this region suggests that the mean numberof different alleles per locus is lower in small popula-tions (Van Rossum et al., unpublished data); furtherresearch must clarify whether there is a link with thereproductive success or seedling recruitment.

Moreover, in some cases there is strong empiricalevidence that population size and isolation may affectinteractions between the plants and flower visitors

(Levin, 1978; Jennersten, 1988; Kwak et al., 1998). Thisplant-pollinator relationship may be very importantsince seed set in primrose and other Primula species isoften already limited by pollination (Piper et al., 1984;Washitani et al., 1994; Matsumura and Washitani,2000). Seed production is thought to be more sensitiveto habitat fragmentation and isolation in heterostylousand dioecious plants than in plants with other breedingsystems because the potential mating partners are morelimited (Levin, 1978; DeMauro, 1993; Agren, 1996).While self-fertilisation occasionally occurs during thelast stages of the flowering period, only cross-pollina-tion between the two morphs is efficient (Woodell, 1960;Ornduff, 1979). This is particularly relevant for many ofthe populations we found in Belgium: we are confrontedwith an increasing difference in pin and thrum numbersin smaller populations due to demographic stochasticitycaused by small sample size (Fig. 10) Normally, pin-thrum ratios fluctuate around 1:1 in large, undisturbedpopulations of primrose (Woodell, 1960; Boyd et al.,1990). However, deviations of this morph ratio havebeen found to be much larger in small than in largepopulations of Primula veris and P. sieboldii and thisimbalance is often associated with a reduction in seedset (Kery et al., 2000; Matsumura and Washitani, 2000).

Another threat to the persistence of the species insuch accessible sites may be the human interest in theattractive and early flowers. According to Rackham(1980), it is hardly conceivable that picking of flowersshould have an appreciable impact in comparison withthe many other hazards to which they are liable, butdigging up the roots could have exterminated small

Fig. 13. Relationship between population size in 1986 and the probability of its survival until 1999 for 34 populations of P. vulgaris in Belgium.

Survival probabilities are calculated with logistic regression. The minimum population size necessary for a 90% survival probability is 95.

22 P. Endels et al. / Biological Conservation 105 (2002) 11–25

populations. In Poland, transplantation experiments aspart of an active protection program failed due to pick-ing of the flowers in early spring or even digging outentire plants for private garden use (Kucharczyk andTeske, 1996). The latter has been observed on severaloccasions for populations near houses in our study area.

4.4. Current legislation and conclusions concerningmanagement of small landscape elements

On a European scale, there has been a steady increasein the production of arable crops (particularly maize).Between 1975 and 1995, there was a 12% decrease in thearea under permanent grassland in the European com-munity Community of nine (Poiret, 1999). However,several measures aim to improve environmental com-patibility of agriculture through changes in land use(Fay, 1999). In particular, most Member States haveimplemented measures for the long term set-aside ofagricultural land to protect water supplies and createbiotope reserves. These so-called agri-environmentschemes aim at low-input farming and an associatedincrease of biodiversity (Bignal, 1998). In England,important changes to the landscape, improvements inhabitats and benefits for several target species have beenrecorded (Ovenden et al., 1998). However, implementa-tion of regulation (EEC) no. 2078/92 has not been asuccess in Belgium: the farmland area covered by agri-environment is still <2% (Fay, 1999).

In Flanders, current legislation is focussing on sus-tainable co-existence of agriculture and nature con-servation in the areas of the supporting network(‘‘IVON’’). However, tools such as voluntary manage-ment agreements with farmers (since September 1999)do not prevent small landscape elements from beingeliminated. In landscapes under intensive agriculturaluse we need a more stringent legislation and control toprotect these natural elements. Stricter regulations con-cerning the management of field edges could be the firststep in attenuating the impact of the surrounding landuse. Buffer zones may need to be 8–20 m wide to mini-mise the effects of herbicide spray drift on plant species(Marrs et al., 1993; Marrs and Frost, 1997), butunsprayed field margins of just 3 m width may reducedrift to the ditches by as much as 95% (de Snoo, 1999).However, to be successful, all these incentives need to fitin a global vision on adequate management practicesand conservation benefits for farmers (Beedell andRemann, 1999).

Acknowledgements

This study was carried out as part of a VLINA(Flemish Impulse Program for Nature Development)project (98/03) and was supported by a IWT (Institute

for Science and Technology) grant. Historical distribu-tion data are used with kind permission of FLO.WER(see Institute of Nature Conservation). We thank Her-man Stieperaere for stimulating discussions and fieldexcursions to some relict populations of Primula vul-garis in the early 1980s. Olivier Honnay, and HermanStieperaere and two anonymous reviewers made valu-able comments on an earlier draft of the paper.

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