Restoration of bracken-invaded Calluna vulgaris heathlands: Effects on vegetation dynamics and non-target species

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available at www.sciencedirect.com

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Restoration of bracken-invaded Calluna vulgaris heathlands: Effects on vegetation dynamics and non-target species Inger Elisabeth Ma˚rena,b,*, Vigdis Vandvika, Kristine Ekelundc a

Department of Biology, University of Bergen, Alle´gaten 41, N-5007 Bergen, Norway Department of Natural History, University of Bergen, Alle´gaten 41, N-5007 Bergen, Norway c The Heathland Centre, Lygra, 5912 Seim, Norway b

A R T I C L E I N F O

A B S T R A C T

Article history:

The coastal heathlands of north-western Europe are endangered habitats of great conser-

Received 27 August 2007

vation value. Invasion by bracken Pteridium aquilinum is a major challenge for conservation

Received in revised form

and restoration of these heathlands, including the under-studied northern regions. Today,

2 January 2008

the herbicide asulam is the most widely applied bracken control measure, but increasing

Accepted 24 January 2008

focus on organic farming and nature conservation calls for alternative, preferably mechan-

Available online 10 March 2008

ical, approaches. In a 7-year replicated field experiment in western Norway, we investigated efficiencies of the four bracken control measures asulam, Gratil, annual cutting and bian-

Keywords:

nual cutting, in restoring the characteristic heathland vegetation structure and species

Asulam

composition. We specifically tested herbicide effects on diversity and composition of

Conservation management

non-target species. Effects of treatments over time were evaluated by repeated measures

Gratil

ANOVA, and for multivariate data, Principal Response Curves. Our results show that UK

Northern heathlands

based control methods are largely applicable to bracken at its northern limit in the Euro-

Organic farming

pean heathland habitat. Asulam resulted in the fastest reduction in cover but cutting

Pteridium aquilinum

proved equally efficient long-term. Community compositions progressed towards desired heathland vegetation, but successional trajectories differed. Asulam had unintended effects on a number of heathland species not predictable by species characteristics or functional groups. Gratil failed to have any long-term effects. In summary, cutting is as efficient as herbicide application in reducing bracken, and more so in restoring northern heathland vegetation over time.  2008 Elsevier Ltd. All rights reserved.

1.

Introduction

The lowland heathlands of Europe are endangered habitats of considerable conservation value (Gimingham, 1992; Aarrestad et al., 2001), now protected under the EU Habitats Directive (92/43/EEC). These are man-made cyclic vegetation systems where secondary succession is manipulated by management, and major threats are abandonment leading

to woodland encroachment, development leading to fragmentation, pollution and subsequent loss of diversity, and invasion of species such as bracken [Pteridium aquilinum (L.) Kuhn]. The recent spread of bracken is recognised as a serious threat to the unique qualities of heathlands as it eliminates characteristic ericoid shrubs, graminoids and forbs by changing the successional dynamics of these semi-natural systems (Watt, 1955; Gimingham, 1972; Kaland and Vandvik,

* Corresponding author: Department of Biology, University of Bergen, Alle´gaten 41, 5007 Bergen, Norway. Tel.: +47 55588136; fax: +47 55589667. E-mail addresses: [email protected] (I.E. Ma˚ren), [email protected] (V. Vandvik), [email protected] (K. Ekelund). 0006-3207/$ - see front matter  2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2008.01.012

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1998; Marrs and Watt, 2006), yielding habitats of low conservation, agricultural and recreational value (Lowday and Marrs, 1992a). Bracken is the most widely distributed Pteridophyte on earth and the only terrestrial fern to dominate large areas outside woodlands in temperate climates (Marrs et al., 2000). Its clones can occupy several hectares, expanding quickly in areas where there is good oxygen supply in the soil and with soil depths >20 cm. An extensive rhizome network works as a store for carbohydrates and contains large numbers of dormant buds (Lowday, 1984). Once bracken is established, slowly-decaying litter (Ghorbani et al., 2006) and potentially toxic compounds (Dolling et al., 1994; Dolling, 1996) may inhibit seed germination, establishment and growth of many characteristic heathland species, including Calluna vulgaris. It is one of a diverse group of species that are able to expand under grazing by combining the ability to maintain dominance at high density with avoidance of grazing (Tryon, 1941; Page, 1976, 1994; Marrs and Watt, 2006). Changes in climate and land use may favour the spread of bracken (Marrs et al., 2000). For example, bracken may benefit from reductions of extensive livestock grazing (cattle effectively trample and also eat some bracken; Williams, 1980; Page, 1982; Pakeman et al., 2005), as well as from recent increases in airborne nitrogen deposition and use of artificial fertilizers (bracken occurs on relatively fertile soils; Miles, 1985). One of the keys to bracken control lays in exhausting the rhizome reserves of buds and carbohydrates (Braid, 1937; Williams and Foley, 1976; Lowday and Marrs, 1992a; Pakeman and Marrs, 1994). Traditionally, bracken was kept in check by grazing and cutting, and fronds used as bedding for livestock. Experiments confirm that biannual cutting can be an efficient control measure (Lowday and Marrs, 1992a, b; Marrs et al., 1993, 1998a; Le Duc et al., 2007). In the 1960s herbicides became widely used in the UK and at present asulam is the most common means of controlling bracken in Europe (Petrov and Marrs, 2000). Recently, asulam’s long-term efficiency has been questioned and multiple follow-up treatments are often recommended (Stewart et al., 2005; Marrs and Watt, 2006; Pakeman et al., 2007). Chemically-based practices also create an ethical dilemma for nature conservation, as well as for farmers aiming to produce e.g., meats, dairy products and honey for the increasing organic market. Norway harbours the northern 1/3 of Europe’s coastal heathlands, characterized by long and unbroken histories of management by means of burning and year-round grazing by sheep of the Old Norse breed (Kaland and Vandvik, 1998; Prøsch-Danielsen and Simonsen, 2000; Vandvik et al., 2005). In contrast to their European Union counterparts, which are protected under the Habitats Directive, these northern heathland habitats lack national legislative instruments to ensure their conservation. Bracken is absent from the northernmost heathlands, but south of ca. 62N it is expanding in heathland areas. However, bracken control has never been studied systematically in these northern heathlands. Asulam is not a legal herbicide in Norway and has never been tested here, but a two-year study of the herbicide Gratil in western Norway (Skuterud, 1998) reported effects comparable to those of asulam in the UK, but with less negative impact on non-target

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vegetation. Both herbicides were therefore included in this study. Most evaluations of different control measures have focused on reducing bracken cover and on restoring heather and a few other flagship species (Pakeman and Hay, 1996; Marrs et al., 1998a, 2000; Mitchell et al., 1998; Pakeman et al., 1998, 2000; Britton et al., 2001). In contrast, nature conservation and organic farming may have more demanding criteria for restoration success, particularly regarding the fates of non-target species (Cadbury, 1976; Pakeman et al., 1997), the rate and direction of revegetation (Pakeman et al., 2007), biodiversity, species composition and other ecosystem characteristics. This calls for more detailed head to head comparisons of different control strategies, in particular different mechanical cutting schemes vs. different chemicallybased strategies (Stewart et al., 2005). In this study we compare the efficiency of different mechanical and herbicide bracken control practices. Our main focus is restoration of the heathland community and potential impacts of herbicides on the species composition and diversity. We ask: (1) How effective are treatments in reducing bracken? (2) How successful are these different control measures in restoring heathland structure and community composition? (3) Do the herbicides affect structure, diversity, or composition of the non-target community? To address these questions we performed a replicated before–after control-impact design experiment and analysed responses over seven years using repeated measurements ANOVAs, redundancy analysis (RDA) and principal response curves (PRC).

2.

Materials and methods

2.1.

Study area

The island of Lygra is situated at 6042’N, and 55’E, in the Lurefjorden fjord basin, approximately 20 km inland from the coast, 40 km north west of Bergen (Fig. 1). Hard and slowly eroding bedrock gives rise to nutrient-poor soils. Climate is oceanic with relatively small differences between June; 12.0 C and January; 2.0 C mean temperatures, the 1600 mm of precipitation is relatively evenly distributed throughout the year (Førland, 1993) and there is a long growing season (ca. 220 days). Lygra is dominated by Calluna/grass heaths with mires/Salix shrubs in wetter areas. Parts of the semi-natural rangeland have been under continuous management (burning, grazing, and turf and heather cutting) up until today, creating a mosaic heathland of different successional stages (Vandvik et al., 2005). The area is grazed by 0.1 cow/ha in summer and by 0.8 sheep/ha in winter (Samson Øpstad; unpublished data), which is comparable to stocking level in other heathland areas (see Hulme et al., 2002). Bracken has increased and by 2004 it had invaded ca. 30% of the area. Experiments were carried out in two adjacent areas; A; invaded by bracken and B; no bracken present. In both areas, ericoid shrub species such as C. vulgaris, Vaccinium myrtillus and V. vitis-idaea occurred throughout, in combination with common graminoids, forbs and mosses. Nomenclature follows Lid and Lid (1994) for vascular plants, Smith (1990) for mosses and Krogh et al. (1980) for lichens.

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Fig. 1 – Location of the island of Lygra in the fjord system of Western Norway.

2.2.

Experimental design

2.2.1.

Herbicide control

Asulam [methyl(4-aminobenzenesulphonyl)carbamate] is a selective post emergent systemic herbicide which controls several annual graminoids, ferns and broad leaved weeds in crop fields by entering the rhizome and accumulating in both active and dormant buds, causing death (Veerasekaran et al., 1976). Bracken frond biomass declines sharply during the two years following treatment but without further management some of the dormant buds and parts of the rhizome survive and it may expand again (Pakeman et al., 2005). Exposure to asulam has shown to inhibit growth of mosses (Rowntree et al., 2003) and as it is a mobile herbicide with high potential for leakage into ground or surface waters, effects on non-tar-

get species are likely and need to be investigated further. Gratil WG 75 (amide sulforon), classified as a sulfonyl urea, is used against Rumex spp. and Ranunculus spp. in fields. It assimilates through foliage and roots, preventing the forming of certain amino acids essential for growth. It does not leak into ground water, but is poisonous for aquatic organisms and can cause long-term damage to aquatic environments (Whitford et al., 2002; Bayer CropScience, 2007). Its systemic effect on the acetolacetate-synthesis terminates growth within 48 h. Wilting of bracken is seen within 2–4 weeks (Skuterud, 1998).

2.2.2.

Experimental design and sampling

Experimental square plots of 25 m2 were established in two areas, A; invaded by bracken and B; no bracken present. The

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latter area was included to enable us to test for herbicide effects on the heathland community, independent of the effect of removing bracken (see below). Plots were placed at least 10 m apart, creating a buffer zone to avoid effects of airborne herbicides (Marrs et al., 1989; Gove et al., 2007). Three 0.5 m · 0.5 m permanent quadrats were randomly placed within each plot. In mid June of year T0 quadrates were analysed for % cover of all species of vascular plants, bryophytes and lichens, functional groups (graminoids, forbs, ericoid shrubs and mosses), and environmental parameters (topography, slope, and aspect). Treatments applications were started in T0 and the quadrats were reanalyzed yearly in July/August of T1–T6. Treatments were randomly allocated to plots within each area according to Table 1. The experimental design was expanded successively over the first three years, yielding a balanced design of four replicate plots · five treatments in area A and four replicate plots · three treatments in area B. In all cutting treatments bracken stems were cut app. 20–30 cm above ground, not affecting the non-target vegetation, and newly cut bracken fronds removed. After initial testing of different cutting techniques (motorised vs. scythes) a long handled scythe was selected as the most efficient tool for our area. In area A, follow-up cutting of emerging bracken fronds in the chemically-treated plots was performed yearly in late July following the methods of Lowday and Marrs (1992a).

2.3.

Data analysis

The final experimental setup is a balanced BACI (before–after, control-impact) design with four replicate plots per treatment, and the general statistical approach chosen was repeated measures ANOVA (Sokal and Rohlf, 1995) for cover data and its multivariate counterpart principal response curves (PRC; van den Brink and ter Braak, 1998; van den Brink and ter Braak, 1999; van den Brink et al., 2003) for species composition data. The general model is y ¼ treatment þ time þ treatment  time with the predictor variables ‘treatment’ and ‘time’ included as factorial variables in all analyses and with different univariate or multivariate response variables (bracken or functional group cover; species composition) depending on the research questions. Because of the successive extensions of the study

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(see above), starting years differed between plots (1997, 1999) resulting in time-series of different lengths. This was accounted for by analysing for effects of treatments as a function of time since treatment, rather than of actual Julian years. This could have been problematic, e.g., if there had been temporal trends of change in the vegetation in our study area due to climate, successional dynamics, or other broadscale factors. We tested this by analysing among-year variation in control plots, and found no significant temporal trends; hence the differing starting years are unlikely to have introduced biases in our results. Repeated measures ANOVA was used to analyse for effects of different bracken control treatments on bracken cover and on the cover of ericoid shrubs, graminoids, forbs, and bryophytes (question 2), using data from the bracken-invaded area A. The analyses were run using the procedure MIXED in SAS 9.1., cover data were arcsine transformed to normalize variances, a first order autoregressive covariance structure across time were used, and error degrees of freedom were estimated by the Satterthwaite approximation (SAS Institute, 2003). In cases of significant treatment effects, differences in the least square means among treatments were tested by post hoc tests, with Bonferroni correction (SAS Institute, 2003). Redundancy analysis (RDA) (RDA; ter Braak, 1987) was used to quantify and visualise effects of the different treatments on the species composition of the community (question 2). The effects of asulam on the non-target community (question 2) were tested by principal response curves (PRC; van den Brink and ter Braak, 1999; van den Brink et al., 2003). PRC is the multivariate equivalent of repeated measures ANOVA, and analyses the community response through time to one or more treatments relative to a control. It is a partial RDA where treatments and time are included as factorial variables in a model analysing the effects of the time · treatment interaction while including time as a covariate to control for any overall temporal trends. Treatment effects (Cdt) quantify the compositional difference between treated plots and controls at each sampling date, and temporal trends can be visualised by plotting Cdt against time. The species scores (bk) can be interpreted as the affinity of each species with this overall effect; species with high positive values follow the overall community response, species with high negative values respond in the opposite way, and species with values near zero do not respond to the treatment. PRCs

Table 1 – Overview of treatments applied to area A (60–90% bracken cover before treatment), and area B (without bracken), four replicates of each treatment x area, a total of 32 plots (96 quadrats) Treatment

Area *

T0

Treatment details Sprayed with 4 kg a.i. ha1 asulox July 31st grazers excluded for 90 days after spraying** Bracken cut annually in late July No treatment applied Bracken cut biannually in mid June and late July Sprayed with 0.06–0.08 kg a.i. ha1 Gratil August 1st Grazers excluded for 7 days after spraying**

Asulam

A,B

1997/1998

9Annual cutting No treatment Biannual cutting Gratil

A A, B A A* , B

1997/1998 1997/1998 1999 1999

T0 = the year treatment was initiated. * Bracken regrowth cut annually in late July following the methods of Lowday and Marrs (1992a). ** Following the prescriptions for use of these herbicides.

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can be tested by Monte Carl permutation tests where whole time-series are permuted freely within areas, and changes in treatment effects through time can be evaluated in sequential tests for each sampling time, permuting the data freely within areas. The analyses were run on log-transformed percentage cover data with down-weighting of rare species (Leps and Sˇmilauer, 2003). Bracken was not included in the RDA or PRC analyses, but was plotted on the diagrams for illustrative purposes. 999 permutations were run in all permutation tests. The software packages CANOCO 4.5 and CanoDraw 4.0 (ter Braak and Sˇmilauer, 2002) were used for analyses and ordination diagrams.

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3.

Results

3.1.

Reducing bracken cover

While untreated plots showed only small non-significant variations in bracken cover over the seven years of recording, all experimental bracken control treatments had strong but variable effects on bracken cover (repeated measures ANOVA: ‘treatment’ effect, d.f. = 17.4, F = 67.9, p(F) = <0.0001; ‘treatment’ · ‘time’ interaction, d.f. = 226, F = 15.9, p(F) < 0.0001; Fig. 2). Herbicides resulted in the fastest reduction of bracken: Under the asulam treatment bracken cover decreased by 99%

a Mean % cover of bracken in quadrats

100 90 80 70 60 50 40 30 20 10 0 T0

T1

T2

T3

T4

T5

T6

T5

T6

Years since onset of treatment

b Mean % cover of ericoid shrubs in quadrat

50

40

30

20

10

0 T0

T1

T2

T3

T4

Years since onset of treatment Fig. 2 – (a) Mean cover (%) of bracken in experimental plots over time. Within each year, filled symbols signify treatments that are significantly different from untreated plots, and different shades signify that the treatment is significantly different from treatments above and below it in the graph at that point in time (P < 0.05 after Bonferroni correction). (b) Trends in mean cover (%) of ericoid shrubs. Treatments; –X– untreated, –d– asulam + annual follow-up cutting, –j– gratil + annual follow-up cutting, –– cut twice yearly, –m– cut once yearly. T0 = year treatment was initiated. (The gratil and cutting twice yearly treatments lasted five years only, any treatment years where n < 3 are not included).

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during the first year after treatment, and the effect persisted throughout the seven years of the experiment. The Gratil treatment, with a 98% decrease, was equally efficient shortterm but after four years the bracken started to recover and it had regained 55% cover after five years. Due to Gratil’s obvious inefficiency in controlling bracken long-term, the full analyses of the effects on the non-target community (questions 2 and 3) are not presented in this paper (although we note that PRC analyses indicate negative effect on Agrostis capillaris, Galium saxatile and Luzula multiflora). Effects of the cutting treatments appeared more slowly, but were equally efficient as asulam in the long run. Biannual cutting reduced bracken cover by 75% the first year, and was indistinguishable from asulam from the second year onwards. Significant effects of annual cutting did not appear until the second year, but they increased gradually over time and were indistinguishable from asulam after five years.

3.2.

Restoring heathland vegetation

0.6

Despite high initial bracken dominance, the vegetation was relatively species-rich with 61 taxa of vascular plants, 23 bryophytes, and two lichens recorded during the seven-year study. The vegetation was dominated by, in order of decreasing mean cover, P. aquilinum (47%), Rhytidiadelphus squarrosus (37%), A. capillaris (25%), Hylocomium splendens (18%), Erica tetralix (17%), C. vulgaris (16%) and Potentilla erecta (14%). A number of less dominant species occurred with high frequency, notably G. saxatile, Anthoxantum odoratum, Deschampsia flexuosa, L. multiflora, Campanula rotundifolia and Carex pilulifera. Treatments induced considerable changes in species composition. The first axis in the treatments · time RDA accounts

T4

-0.4

RDA axis 2 (5.4%)

Hylo spl

-0.6

T0 T6

Pter aqu Agro cap T0 T0

T0

Anem nem Oxal ace Viol pal Gali sax Dact mac Luzu pil Agro can Rhyt squ Vacc myr Pote ere Anth odo Hypn jut Poly com Pseu pur Achi mil Fest viv Pleu sch Vacc v-i Dant dec T6 Lotu cor Care pil Call vul Hype pul

T6

Euph mic

RDA axis 1 (9.9%)

0.8

Fig. 3 – Multivariate redundancy analysis (RDA) ordination diagram of species and bracken control treatments through time for the heathlands at Lygra, Norway. Compositional change within the different treatments over the course of seven years (cut twice; five years) is drawn as trajectories where T0 demarks the year treatment was initiated, and T6 (cut twice; T4) demarks the last year of treatment. Treatments; –X– untreated, –d– asulam + annual follow-up cutting, –– cut twice yearly, –m– cut once yearly. Species names abbreviations are the four + three first letters of the genus and species names, respectively.

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for 9.9% of the total compositional variability in area A and reflects a general successional trend in the treated plots away from the controls (Fig. 3). This trend is associated with increasing abundance of a large number of species including ericoid shrubs, graminoids, forbs and bryophytes, and decreasing abundance of only one species, A. capillaris, in addition to the treated species P. aquilinum. The second RDA axis (5.4% of the variability) mainly reflects differences in starting conditions between blocks. In contrast to the strong floristic responses we found no overall treatment effects on relative abundances of the different functional groups (forbs, graminoids, ericoid shrubs, mosses) (repeated measures ANOVAs; P > 0.05 after Bonferroni correction for ‘treatment’ effects and ‘treatment’ · ‘time’ interactions in all cases), suggesting that species within each of these groups respond individualistically to the treatments. The observed changes in species composition combine two processes; establishment of new individuals (from dispersal or soil seed bank) and increased cover of individuals already present at onset of the experiments. For ericoid shrubs, which are of particular interest in heathland restoration, we found that while these species increased in cover over time in treated plots where they were initially present (Fig. 2b) colonization of new plots was rarely observed (only 5 cases during the course of the study). This increases variability between replicate treated plots over time, which may contribute to the lack of significant responses in terms of functional group cover in our experiments (e.g., Fig. 2b).

3.3.

Effects of asulam on non-target species

The PRC diagrams (Fig. 4) focus on the effects of asulam on the non-target plant community by contrasting successional trends in the asulam-treated areas with unsprayed areas. To evaluate the herbicide effect per se, the annual cutting treatment was used as control in this analysis. The treatment effects (Cdt) quantify the compositional difference between plots and controls at each sampling date, and temporal trends are visualized by plotting Cdt against time (Fig. 4). Here, species with high positive bk weights follow the overall community response, and are negatively affected by the asulam treatment; V. myrtillus, Euphrasia micrantha, Achillea millefolium, Pleurozium screberii, Rumex acetosa, Danthonia decumbens, Polytrichum commune and Pseudoscleropodium purum, in addition to P. aquilinum. C. vulgaris was also negatively affected. However, the majority of the non-target species actually responded positively to the asulam treatment. The treatmentcontrol contrast in these areas (Fig. 4a) reflects the joint effect of decreased bracken cover and spraying. To tease apart these effects, we specifically tested the effect of asulam sprayed directly on the non-target community in the area with no bracken; B (Fig. 4b). This resulted in significant effects on a similar number of species, but here the effect of the herbicide was predominately negative, hence high positive bk weights for species like A. capillaris, A. odoratum, Veronica officinalis, G. saxatile, Juncus squarrosus, Circium palustre, Lotus corniculatus, Ranunculus acris, H. splendens, Viola palustris, Holcus lanatus, Trientalis europaea and P. erecta. In both analyses, there was a significant compositional response to spraying in the first

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Fig. 4 – PRC diagrams and species scores (bk) on PRC axis 1, showing the overall impact of asulam on heathland species composition (treatment effects; PRC axis 1 or Cdt) relative to; (a) unsprayed cut once (controls) in bracken-invaded heath and (b) unsprayed in heath without bracken. The responses (bk) of individual species are shown to the right: high positive bk values indicate the species’ response to be well described by the PRC, i.e. decrease in the sprayed areas, high negative values are indicative of species that increase in sprayed areas. Only species with relatively strong responses are shown, species with bk values near 0 are not significantly affected by the treatment. *Significantly different from the control, P < 0.05, **Significantly different from the control, P < 0.001. Species listed above the dotted line to the right are negatively affected by the asulam treatment, and species below it are positively affected.

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years after treatment, an effect that weakened and disappeared within 2–5 years.

4.

Discussion

4.1. Mechanical versus herbicide treatment; what works best and when? This paper presents the results of different bracken control treatments on bracken cover, non-target species and vegetation dynamics to help assess the role of herbicide versus mechanical control, especially with regard to organic farming and nature conservation. We found that all treatments reduced bracken significantly during the course of the test period, but that the response rates differed considerably. Biannual cuttings or spraying with asulam followed by annual cutting were the most effective means of reducing bracken cover long-term, confirming that previously reported high efficiency of these measures (Lowday, 1984; Marrs et al., 1993, 1998a; Paterson et al., 1997; Le Duc et al., 2007) also holds true for northern heathlands. Yearly cutting took longer to take effect, as one might expect, but once it did it was as effective as cutting biannually. As asulam is not legal in Norway, and as Gratil has been recommended as an alternative to asulam based on one short-term (2-year) experiment (Skuterud, 1998), it was of interest to include Gratil into the experimental protocol. In doing so, we also highlight the importance of long-term monitoring in researching vegetational change, as called for by Stewart et al. (2005). However, our results show Gratil sprayed bracken to regain dense cover the third year after treatment and can not be recommended as a bracken control tool. This recovery, in spite of followup cutting, is difficult to explain and should be addressed in further investigations.

4.2.

Do we restore heathland after bracken control?

All bracken control treatments affected species composition, inducing a shift towards more open and species-rich communities dominated by ericoid shrubs, graminoids, and forbs (Fig. 3). We found more species benefiting from the removal of bracken than suffering from the treatments, such as Hypericum pulchrum, C. pilulifera, V. officinalis, Conopodium majus, L. corniculatus, Festuca vivipara and Vaccinium vitis-idaea. Some previous attempts at restoring Calluna heathlands by bracken control in the UK have resulted in grass-dominated communities, and simply controlling bracken by herbicides may not result in conservation or restoration of Calluna heathlands (Pakeman et al., 1997).This seems not to be the case at our site. The grazing regime at the site (sheep and cattle) is one possible explanation as Williams (1980) found bracken regrowth after asulam application to be considerably slowed by grazing sheep and cattle compared to sites grazed by sheep alone. Hence, trampling by cattle can be an important factor in bracken control, at least in areas where bracken stands are not too dense. Our use of follow-up annual cutting treatments may also have increased the rate of success in reestablishing desirable heathland vegetation (see also Lowday and Marrs, 1992a; Marrs et al., 1998b).

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4.3.

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Do herbicides affect non-target species?

In the bracken-dominated area the majority of non-target species were positively affected by asulam, suggesting the herbicide to have little detrimental effect on biodiversity. However, this effect confounds two causal factors: the herbicide per se and its effect through the removal of bracken fronds. Treatments in the area lacking bracken were included in the experimental setup to tease apart these two effects. Here, a majority of species were negatively affected, suggesting asulam to have negative effects on the biodiversity of nontarget communities. A dense cover of bracken fronds will act as an umbrella, somewhat protecting the underlying vegetation from the full effects of the chemicals. However, the topography, vegetation cover and bracken density of northern heaths are very heterogeneous and herbicide application will unavoidably result in non-target species being sprayed directly. This calls for caution in herbicide application in heterogeneous heathlands, as found in northern regions, where non-target communities are intermingled with bracken-invaded heath (Vandvik et al., 2005). The negatively affected species belonged to different taxonomic and functional groups, and include the graminoids A. capillaris, Anthoxanthum odoratum, J. squarrosus and H. lanatus, the forbs V. officinalis, G. saxatile, L. corniculatus, V. palustris, T. europaea and P. erecta, the ericaceous dwarf-shrub V. myrtillus, and the mosses H. splendens and Psuedoscleropodium purum. A number of additional species showed negative trends but occurred too sparsely to prove statistical significance. V. myrtillus and P. purum were negatively affected in both areas and might be particularly sensitive to asulam. Other species found to be asulam sensitive are Digitalis purpurea, Prunella vulgaris, Lychnis flos-cuculi and Centaurea nigra (Marrs et al., 1986). A particularly interesting group of species are those unaffected or showing a positive response in area A, yet negatively affected in area B, such as V. officinalis and L. corniculatus. This apparent shift can be accounted for by the ‘dual effect’ of asulam in the bracken-dominated area where the positive effect of its removal cancels out the negative effect of the herbicide per se. By including this ‘double control-method’ in our experimental setup, we are able to identify this group of bracken-suppressed, yet herbicide-sensitive species. Such species may be particularly difficult to restore by chemical control, especially if repeated spraying is part of the protocol. This study was carried out on a small scale in vegetation dominated by common species. Species negatively affected by the herbicides belonged to different taxonomic and functional groups, making generalisations of potential responses of other (groups of) species very difficult and need further investigation. In particular, many ferns are sensitive to asulam (Pakeman et al., 2000), and particular care should be taken in areas with a diverse and/or threatened fern flora.

4.4.

Implications for management and conservation

As most studies of herbicides are conducted in the fields of agriculture, forestry or by the manufacturers, they yield little information on the effects of these herbicides on semi-natural vegetation for conservation or restoration purposes. While much is known about the effects on target species, there is

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less information regarding their effects on non-target vegetation dynamics and on endangered or vulnerable non-target species likely to be found in heathlands (Marrs, 1985). For successful conservation management these effects should be of most important consideration (Critchley et al., 2004; Bremner and Park, 2007). For organic farming, which preclude the use of chemical control, alternative control methods need to be formulated. Our work shows that biannual cutting retards regrowth sufficiently for effective control. Annual cutting was nearly as efficient as biannual cutting after five years, and may be a more economic option long-term. It is not possible to eradicate the species permanently; Marrs et al. (1998a) did not succeed in this even after 18 years of continued bracken control, but the population can be kept at a level acceptable for keeping grazing livestock and conserving the threatened habitat of coastal heathlands. All bracken control measures were more efficient in reducing bracken cover and had longer-lasting effects in this study compared to studies further south in Europe (e.g., Lowday and Marrs, 1992a; Marrs et al., 1998a). This could be due to climatic and environmental constraints at the northern brink of bracken’s distribution in the heathland habitat, suggesting that bracken control may be easier and less labour intensive here. On the other hand, bracken shows strong plastic responses to yearly climate variability (Le Duc et al., 2003). In northern areas, where temperature is the main limiting factor for growth, future increases in temperature and growing season duration could imply range expansion, increasing rates of bracken invasions and denser bracken stands in alreadyinvaded areas (Marrs et al., 2000; IPCC, 2007). Future climate change could therefore result in a greater need for bracken control measures in the management of northern heathlands. In conclusion, we note that selection of bracken control measures for heathland conservation, restoration or management needs to take into account regional location and topography, the desirable future vegetation after control as well as any special needs of particular land-uses such as organic farming, habitat conservation or conservation of rare/endangered species. Mechanical control can be relatively efficient, especially in northern areas when combined with grazing. These are important issues as it is likely that the use of bracken control measures will have to increase if the heathlands of Northern Europe are to be conserved for the future.

Acknowledgements We thank P.E. Kaland for initiating the project, V. Dahl, J. Wilhelmsen and M. Kvamme for field assistance, E. Heegaard for identifying bryophytes and lichens, B. Helle for technical assistance, and two anonymous referees for constructive comments. This work was funded by the Agricultural board of Hordaland, the University of Bergen, Grolles legat and Bergen Myrdyrkningsforeningsfond.

Appendix A Species names in full and abbreviated species names; the four + three first letters of the genus and species names,

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respectively, for the 86 species recorded during the seven-year study. Abbreviations are used in Fig. 3. Species names

Abbreviation

Achillea millefolium Agrostis canina Agrostis capillaries Anemone nemorosa Anthoxanthum odoratum Betula pubescens Blechnum spicant Brachythesium rutabulum Bryum spp. Calluna vulgaris Campanula rotundifolia Campestris spp. Carex nigra Carex ovina Carex pallescens Carex pilulifera Cerastium fontanum Ceratodon purpureus Circium palustre Cladonia spp. Conopodium majus Cornus suecica Dactylorhiza macultaa Danthonia decumbens Deschampsia cespitosa Deschampsia flexuosa Dicranella spp. Dicranum scoparium Dicranum spurium Empetrum nigrum Erica tetralix Euphrasia micrantha Festuca rubra Festuca vivipara Galium saxatile Hieracium pillosella Holcus lanatus Hylocomium splendens Hypericum pulchrum Hypnum jutlandicum Hypochaeris radicata Juncus conglemoratus Juncus squarrosus Juniperus communis Leontodon autumnalis Leucobryum glaucum Lophocolea bidentata Lotus corniculatus Luzula pilosa Luzula spp. Mnium hornum Nardus stricta Oxalis acetosa Peltigera spp. Plantago lanceolata

Achi mil Agro can Agro cap Anem nem Anth odo Betu pub Blec spi Brac rut Bryu spp. Call vul Camp rot Camp spp. Care nig Care ovi Care pal Care pil Cera fon Cera pur Circ pal Clad spp. Cono maj Corn sue Dact mac Dant dec Desc ces Desc fle Dicl spp. Dicr sco Dicr spu Empe nig Eric tet Euph mic Fest rub Fest viv Gali sax Hier pil Holc lan Hylo spl Hype pul Hypn jut Hypo rad Junc con Junc squ Juni com Leon aut Leuc gla Loph bid Lotu cor Luzu pil Luzu spp. Mniu hor Nard str Oxal ace Pelt spp. Plan lan

B I O L O G I C A L C O N S E RVAT I O N

Appendix A – continued Species names

Abbreviation

Pleurozium schreberii

Pleu sch Poa spp. Pohl spp. Poly ser Poly com Poly jun Poly pil Pote ere Pseu pur Pter aqu Raco aci Raco lan Ranu acr Rhyt lor Rhyt squ Rume ace Rume acl Sali cap Sali rep Sorb auc Tara col Trie eur Trif rep Ulot cri Vacc myr Vacc uli Vacc v-i Vero off Viol can Viol pal Viol riv

Poa spp. Pohlia spp. Polygala serpyllifolia Polytrichum commune Polytrichum juniperinum Polytrichum piliferum Potentilla erecta Pseudoscleropodium purum Pteridium aquilinum Racomitrium aciculare Racomitrium languinosum Ranunculus acris Rhytidiadelphus loreus Rhytidiadelphus squarrosus Rumex acetosa Rumex acetosella Salix caprea Salix repens Sorbus aucuparia Taraxacum coll. Trientalis europaea Trifolium repens Ulota crispa Vaccinium myrtillus Vaccinium uliginosum Vaccinium vitis-idaea Veronica officinalis Viola canescens Viola palustris Viola riviniana

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