Structure and Diversity of Erica Ciliaris and Erica Tetralix Heathlands at Different Successional Stages After Cutting

Journal of Environmental Management 94 (2012) 34e40

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Journal of Environmental Management

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Structure and diversity of Erica ciliaris and Erica tetralix heathlands at different successional stages after cutting

A. Muñoz a,*, J. García-Duro a, R. Álvarez a, X.M. Pesqueira a, O. Reyes a,b, M. Casal a a Departamento de Bioloxía Celular e Ecoloxía, Facultade de Bioloxía, Universidade de Santiago de Compostela, 15782 Campus Sur, Santiago de Compostela, Spain b Departamento de Bioloxía Celular e Ecoloxía, E.P.S. Universidade de Santiago de Compostela, Campus de Lugo, 27002 Lugo, Spain article info abstract

Article history: In NW Europe, it is known that cutting is a useful tool for managers with regard to decisions about the Received 4 October 2010 conservation and management of wet heathlands. Nevertheless it is rarely described quantitatively in the Received in revised form international literature. In Spain, knowledge about this is scarce or lacking. In this study, twenty 19 July 2011 communities were selected in Galicia (NW Spain) that would represent from one to four stages of Accepted 5 August 2011 vegetation development after cutting. Two 5 5 m plots were established for each stage to characterise Available online 22 September 2011 the vegetation on the basis of its species composition, frequency values, vertical structure and linear cover features. The Diversity Shannon index was calculated and multivariate analyses were performed. Keywords: Wet heathlands As succession advanced, notable changes were produced in the cover of dominant species, Erica ciliaris fi Management and Ulex gallii in the rst stages and Erica tetralix and Genista berberidea in mature ones. Also, the species Autosuccession richness decreased because of the reduced number of herbs species in the mature stages and, finally, the Life forms cover values are indicators of the degree of vegetation development, together with the other parameters Species richness of height, overlayering or diversity. Cutting is a useful tool for management of heathlands because the Multivariate analysis existence of vegetation units belonging to different succession stages increases the internal diversity of communities. On the other hand, the vertical and horizontal structure reflects the formidable resilience of the vegetation community to this practice. This study offers a global vision of the dynamics of wet heathlands after cutting, with very useful ecological information that can be used by the people responsible for their management. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction There exists at the present time a large number of scientists, managers, associations and government bodies interested in the There are a large number of techniques that can be used by recovery and conservation of the wet heathlands. managers in the management and conservation of heathlands to The ecological study of the wet heathlands successional stages improve their structural diversity (Liley, 2005; Webb, 1998). In SW and their characteristics of structure, composition and dominant Europe, including Galicia, cutting is the most characteristic tradi- species in relation to cutting is useful to the managers for identi- tional method (Gimingham and Smidt,1983; Marey et al., 2006)and, fying the types of vegetation that are being managed in order to together with cultural burning and grazing, is considered to be one of dedicate them to social usage, habitat conservation, resource the possible causes originating shrubland communities. This conservation for the fauna, to avoid propagation of fire, to avoid anthropic activity has been a widely extended practice in the tradi- collapse through transformation into woodland, and to maintain tional agriculture of Western Europe for centuries, but has decreased the high ecological and cultural value of these communities. considerably since the middle of the XX Century (Gimingham, 1972). Erica ciliaris and Erica tetralix communities are found on flat These cultural heathlands were managed by hand cutting, grazing or ground with poor drainage and a positive hydric balance, which are burning in the last centuries, but the lack of management is swamped during 6e9 months of year. These communities have provoking their disappearance. Therefore, they should be integrated a great ecological importance (high species richness and diversity, in conservation plans that contemplate sustainable management. acting as hydrological control, carbon sink and palaeontological files), scientific research, educational and cultural. Also, they are small communities and isolated from each other and have a high * Corresponding author. Tel.: þ34981563100x13318; fax: þ34981596904. risk of collapse, with several exclusive species. Their conservation is E-mail address: [email protected] (A. Muñoz). considered to be a priority in Appendix I of the Habitats Directive

(92/43/EEC; H4020: Temperate Atlantic wet heaths with E. ciliaris 1 stage 2 stages and E. tetralix). Despite the imperative necessity of ecological knowledge about the succession after cutting in the E. ciliaris and E. tetralix heathlands, there is very little quantitative information available. For this reason, the main objective of this study is to analyse the principal structural and compositional changes of these communities and in the abundance of the dominant species during the succession process after cutting. 3 stages 4 stages

2. Materials and methods

2.1. Field methods

A total of 20 sampling sites situated in Galicia, NW Spain (Fig. 1), were selected. The annual rainfalls vary within a range of 1300e2000 mm, being higher in the more westerly communities, whilst average temperatures vary between 10 and 14 C, with Fig. 2. Diagram of location of two plots (5 5 m) in the communities with 1, 2, 3 or 4 minimums higher than 6 C and maximums of less than 19 C stages. (Ninyerola et al., 2005). The selected sampling sites had evident signs of hand cutting as the latest disturbance and they presented between one and four stages of vegetation development. Succes- 2.2. Data treatment sional stages were established as a function of the vegetation height, considering this variable to be an indicator of the time elapsed after The contribution of each group (Tree, Shrubs, Perennial Herbs the last cutting (Puentes and Basanta, 2002). The stages were and Annual Herbs) to the total sum of frequencies was calculated delimited in the following manner: Stage 1: 0e30 cm; Stage 2: using the total frequencies of each species obtained. With the linear 30e60 cm; Stage 3: 60e90 cm and Stage 4: >90 cm (Table S1). cover data, the percentages of Leguminosae, Ericaceae, other woody In each stage, two 5 5 m plots were established over homoge- species and herbs were calculated, together with the percentage of neous and representative vegetation, in order to characterise the overlayering of the woody species using the formula proposed by vegetation according to different variables, being the final data the Basanta et al. (1988). Diversity Shannon Index (H0) was calculated for average of them both (Fig. 2). An inventory of Species Composition the woody species linear cover data and the cover of Herbs. was made (Table S2). The Frequency Values were calculated from the Finally, two, Redundancy Analyses (RDA) were applied, presence-absence data for each of the woody and herbs species including Successional Stages as an independent and discrete obtained using a 30 30 cm quadrate placed randomly 30 times in variable (Ewing et al., 2007; Colombaroli et al., 2009; Jones et al., each plot. To determine the vertical structure, the percentage occu- 2011). The first one was applied to the cover data of the variables pied by the vegetation was estimated at 6 previously established that were present in more than 10% of the samplings, such that the vertical layers (Godron et al., 1968,modified by Basanta et al., 1988). data matrix was formed by the 36 cases corresponding to samples The Linear Cover was measured using a total of 25 m per plot. The and 18 variables corresponding to the cover values of woody centimetres occupied in each line by each woody species and no species, Herbs and Bare Ground. The second RDA was applied to the woody cover (NWC), which includes Herbs and Bare Ground, were structural variables data and the matrix was formed by the 36 cases noted. The cover of Herbs was taken as a single variable, without and 11 structural variables: Average vegetation height, Number of differentiating the species. Only when there was no overlayering of woody species, Number of herbs species, Woody Coverage, No woody vegetation was the ground considered to be Herbs or Bare Woody Coverage, Diversity, Overlayering and frequency (%) of Ground. Trees, Shrubs, Perennial Herbs and Annual Herbs.

Fig. 1. Map of location of the sampling sites in Galicia (NW Spain). 36 A. Muñoz et al. / Journal of Environmental Management 94 (2012) 34e40

To detect significant differences between stages, ANOVA The results show that Ericaceae family dominates significantly (Overlayering) and KruskaleWallis analysis (Life Forms, Vertical in all stages, with values that vary between 40 and 60% Layers, Cover and Shannon Index) were applied. (30.8 > c2 > 19.9, d.f. ¼ 3; p ¼ 0.00). It is followed by the Legu- minosae family, which presents values of between 30 and 40% in 3. Results the first three stages, decreasing in Stage 4 to 20%. Herbs showed their maximum cover in Stage 1(16.4%), while the group of Other 3.1. Life forms Woody Species significantly increased its cover value (c2 ¼ 13.2, d.f. ¼ 3; p ¼ 0.00) in Stage 4 reaching the 17.9%, due, above all, to There is an almost total dominance of Shrubs in the four stages Myrica gale cover (Fig. S1). studied (Table 1), with average frequency values that vary between An analysis at the level of species reveals that, in the Stage 1, 43 and 57%. The Shrubs are prevailed over by the Perennial Herbs in E. ciliaris (38.3 8.6%), Ulex gallii (33.5 7.6%) and E. tetralix Stage 1 (53.8 6.2%) and Stage 2 (50.0 3.1%), the average (20.1 8.1%) present a higher percentage of cover value, whilst frequency values of which progressively changes in the following other woody species, such as Calluna vulgaris, Frangula alnus, Erica stages, reaching its minimum in Stage 4 (35.6 6.1%). With regard cinerea or Salix atrocinerea, do not reach 5%. The same three woody to the Trees, their average frequency value increases in the stages of species, with higher values, dominate in Stage 2, but the cover of major vegetation development (c2 ¼ 13.6, d.f. ¼ 3; p ¼ 0.00), but E. ciliaris and U. gallii decreases significantly in the more advanced they never have more than 10% of abundance in any of these stages. stages, showing values of 12.1 5.1% (c2 ¼ 10.5, d.f. ¼ 3; p ¼ 0.02) Lastly, the group of Annual Herbs has the lowest abundance in all and 1.6 0.9% (c2 ¼ 15.0, d.f. ¼ 3; p ¼ 0.00), respectively, in Stage 4 stages (<1.5%) and is null in Stage 4. (Fig. 4). The opposite is found in the case of E. tetralix, its cover In almost all stages (Table 1), the Perennial Herbs show the changes progressively as time passes, converting it into the domi- highest number of species and they decrease significantly from nant species in the final stage studied with an average cover value 10.8 1.5 to 7.0 2.6 as the community matures (c2 ¼ 8.8, d.f. ¼ 3; of 59.2 13.8%, together with Genista berberidea (28.2 9.5%; p ¼ 0.03), showing the lowest number in Stage 4. In the last two c2 ¼ 13.9, d.f. ¼ 3; p ¼ 0.00), which in the previous stages had stages these values equalise with respect to the number of Shrubs a much lower cover value. During the succession, the number of species (4.3 0.2e6.1 0.7) which shows little variation over all woody species remains practically constant but an increase in cover four stages, contrary to the number of Trees species that is low in of E. tetralix or two species is observed, which become dominant the first three stages (<1), but increases in Stage 4 (3.0 0.7; and in the case of co-domination would either be accompanied by c2 ¼ 13.2, d.f. ¼ 3; p ¼ 0.01). The number of Annual Herbs species is G. berberidea or M. gale. minimal (<0.5) and null in Stage 4. There are significant differences between the different life 3.4. Diversity measurements forms, both in the percentages of relative frequencies and in the number of species, in each one of stages (30.1 > c2 > 17.6, d.f. ¼ 3; The total species richness inventoried is 84, 23 woody species p ¼ 0.00). The Shrubs and Perennial Herbs have the highest values. and 61 herbs species (Table S2). The results reveal that there are no Moreover, as the succession advances, the differences between significant differences between stages. The stage with the highest these two groups increase. number of species is Stage 1 (17.8 2.1 spp/25 m2), followed closely by Stage 2 (17.3 2.3 spp/25 m2), with little variations in Stage 3 3.2. Vertical structure (12.5 0.7 spp/25 m2) and in Stage 4 (14.9 2.0 spp/25 m2). This change is due to the initial number of herbs species, which is less in The vertical structure in Stage 1 shows cover values of higher mature stages (Table S1). The diversity values (H0) obtained from than 75% in the first two layers established (0e25 cm), with very the linear cover data shows there are not significant differences, little Bare Ground (Fig. 3). With the succession advance, Layer III because the values remain practically constant along the succession (25e50 cm) increases its cover (c2 ¼ 21.3, d.f. ¼ 3; p ¼ 0.00), (Stage 1 ¼ 1.5 0.5; Stage 2 ¼ 1.7 0.1; Stage 3 ¼ 1.8 0.5 and reaching 85% in Stage 2 and presents the highest degree of cover of Stage 4 ¼ 1.7 0.6). all the defined layers in Stage 3. In the last stage, the cover in Layers III and IV is higher, with values of between 90 and 100%, which 3.5. Relationship between the species and structural variables and presents a significantly higher coverage (c2 ¼ 34.8, d.f. ¼ 3; stages p ¼ 0.00). Since the RDA’s only computed a single RDA axis, in the first one, 3.3. Linear cover of woody species applied to the cover data, a correlation of 0.6 exists between the dependent variables (cover data of species) and the independent Woody species increased in cover as the community matured, one (Successional Stages) in Axis I and none in Axis II, explaining leading to significantly increased overlayering (F ¼ 5.6, d.f. ¼ 3; the Axis I the 100% of variance of the specieseenvironmental p ¼ 0.04) of the cover of different species, from Stage 1 (16.7 3.8%) relation. The Montecarlo test reveals that the species cover and the to Stage 4 (47.0 9.7%). development stage are significantly related (p ¼ 0.00). The total of

Table 1 Average value and standard error of the relative frequency and of the number of species/25 m2 of each biological type (Tr ¼ Trees, Sh ¼ Shrubs, PH ¼ Perennial Herbs, AH ¼ Annual Herbs) in the four succession stages. The biological types which change their values over the stages are marked with *.

Stage Relative frequency (%) Species number/25 m2

Tr Sh PH AH Tr Sh PH AH 1 0.7 0.4 43.4 6.8 53.8 6.2 0.3 0.2 0.7 0.3 5.9 0.7 10.8 1.5 0.4 0.3 2 1.2 0.6 48.5 3.1 50.0 3.1 0.2 0.1 1.1 0.4 6.1 0.7 9.9 1.4 0.3 0.2 3 2.8 1.6 57.2 4.8 38.5 5.1 1.5 1.1 0.5 0.2 4.8 1.5 7.0 2.2 0.2 0.1 4 7.9 1.8* 53.8 6.8 35.6 6.1 0 3.0 0.7* 4.3 0.2 7.0 2.6* 0 A. Muñoz et al. / Journal of Environmental Management 94 (2012) 34e40 37

Fig. 3. Horizontal occupation (average & standard error) of the vertical layer deﬁned, in each of the stages of succession studied. samplings performed are distributed along a vegetation cover gradient (Fig. 5), such that the samples situated on the extreme 0. 1 right-hand side of the graph are characterised by the cover domi- Ecil nance of E. ciliaris, U. gallii, Herbs or Bare Ground, whilst in the Ugal samples situated towards the left-hand side E. tetralix and G. berberidea dominate, which indicates that there is variability in the vegetation composition of these samples. M. gale appears in the Ueur more mature stages of succession. In the RDA applied to the Rub structural variables (Fig. 6), there is a correlation of 0.4 between the Dcant Ldif dependent variables and the variable Successional Stages in Axis I Ecin Epol

Faln Succesional Stages Bare Ground Axis II Bpen

Cvul Gberb Satr Mgal Srep

Herbs Etet 8.0-

2.1- 6.0 Axis I

Fig. 5. Redundancy Analysis biplot applied to cover data. Herbs, Bare Ground and the woody species are represented: Betula pendula (Bpen); Calluna vulgaris (Cvul); Daboecia cantabrica (Dcant); Erica ciliaris (Ecil); Erica cinerea (Ecin); Erica tetralix (Etet); Euphorbia polygalifolia (Epol); Frangula alnus (Faln); Genista berberidea (Gberb); Lith- Fig. 4. Cover values of dominant woody species (average & standard error): Erica cil- odora diffusa (Ldif); Myrica gale (Mgal); Rubus sp.(Rub); Salix atrocinerea (Satr); iaris, Erica tetralix, Genista berberidea and Ulex gallii. S. repens (Srep); Ulex europaeus (Ueur); U. gallii (Ugal). 38 A. Muñoz et al. / Journal of Environmental Management 94 (2012) 34e40

0.1 et al., 2005). However, it must be noted that the number of perennial herbs species is greater than that of shrubs, whilst the NWC annual herbs are practically non-existent, results that coincide with PH those of other authors (Basanta et al., 1989). This abundance of Herbaceae converts Stage 1 into the appropriate habitat for grazing and recreation. HS Cutting generally affects the epigeous vegetation community and generates a subsequent intense growth of many species and different families. E. tetralix heathland is characterised by the high cover and stratiﬁcation values of the shrub species, and by scarce areas that are bare of woody species and generally occupied Succesional Stages by herbs species. These communities show very dense vegetation Axis II Height with co-dominance of E. ciliaris, E. tetralix, G. berberidea and U. gallii. WS Both of these results were also obtained by Basanta et al. (1989). Tr Diversity The cover of the vertical layers recover rapidly after cutting, as in Stage 1 the quantity of NWC is very low. The frequency of this AH disturbance inﬂuences in the amount of NWC (Liley, 2005). In the past, these communities were cut by hand at any time of the favourable season of the year, in management cycles of 7e8 years and were also grazed. At the present time use for grazing is sporadic Sh Overlayering and rare, and so turns of hand or mechanised cutting (Photo S1 and Photo S2) and burning are stretched to 10e20 years (E. Ferreira,

0.1- personal communication). A greater frequency of cutting in WC a community produces an increase in NWC, thus permitting the 6.0- Axis I 2.1 establishment of a greater number of woody and herbs species, such as “transient species” (Grime, 1998) incoming from adjacent Fig. 6. Redundancy Analysis Biplot applied to structural variables. The structural communities. The woody species are dominant from the first variables are: Height, Number of woody species (WS), Number of herbs species (HS), stage, increasing their cover as time passes, as was found by Calvo Woody Cover (WC), No Woody Cover (NWC), Diversity, Overlayering, and frequencies et al. (2002b, 2005). In E. ciliaris and E. tetralix communities, (%) of Trees (Tr), Shrubs (Sh), Perennial Herbs (PH) and Annual Herbs (AH). Ericaceae family shows the greatest amount of cover, followed by Leguminosae, like Basanta et al. (1988). In Cantabrian heathlands, a dominance of U. gallii was observed after mechanical clearing and none in Axis II, explaining the Axis I the 100% of variance of the because of its better resprouting ability compared with heather e species environmental relation. The Montecarlo test reveals that species (Celaya et al., 2007). The increase of cover is different fi the species cover and the development stage are signi cantly depending on the specific woody species. U. gallii and E. ciliaris ¼ related (p 0.01). The result indicates that incipient stages are reach their maximum cover in the first stages and then decrease in characterised by the presentation of a high number of herb species, the mature stages, whilst the cover of E. tetralix and G. berberidea mainly Perennial Herbs and a greater cover value of NWC. Whereas, increases from the first stage until it reaches its maximum values in mature stages (Stages 3 and 4) are characterised by their greater Stage 4. According to the Mass Hypothesis of Grime (1998), the cover values and number of woody species, dominance of the functioning of ecosystems is determined by the trait values of Shrubs (even though the Trees are important in some samples from dominant species. The studies of Garnier et al. (2004) and Wright these stages) and higher values of diversity and height. et al. (2004) reveal that the functional leaf traits are significantly fi The principal separation of the variables in both RDA is ful lled related to the functioning of ecosystems. Specifically, Garnier et al. by Axis I, which represents the temporality. This differentiates the (2004), when studying old fields, found that plant traits change communities studied as much at the species covers level as in their with the age of the community and that there is a replacement of structural aspect. fast growing species, which dominate in the early stages, by species with slower growth rates that tend to economise the available 4. Discussion resources better. In our case, the four dominant species are shrub species with small leaves and/or spines that have an intermediate E. ciliaris and E. tetralix heathlands show a fairly characteristic leaf mass value per area. The Leguminosae fix nitrogen and, for this qualitative and quantitative composition, which differentiates reason, the content of this element is two or three times higher them from the rest (Basanta et al., 1989; Rodríguez Oubiña, 1987). than in the Ericaceae, but this is the only important difference. As The hand cutting triggers the secondary succession process. The the succession advances, the change in the dominant species analysis of Life forms shows a characteristic general pattern, with produced as these communities mature do not show any changes in a greater abundance of Shrubs in all stages excepting Stage 1, in the foliar characteristics of the community, because the increase of which the Perennial Herbs dominate. Most of the species that are leaf mass per area and of the total leaf nitrogen is related to the present are perennials, adapted to swamping, whilst the number of increase of the biovolume of these species (Muñoz, 2009) and to annual species is very low or null. The specialist species are more changes in the leaves. This is probably because it is a secondary affected than the generalists by the loss of their habitat (Warren succession and the changes are small, or also because the time et al., 2001). However, when the specialist plants are perennials, elapsed between the four stages is not sufficient to reflect in the they can persist for some years in small populations, thus post- foliar characteristics of the community, which are modified later by poning their extinction (Oostermeijer et al., 1994). This could be the entrance of wide leaf tree species and different foliar charac- because the perennial species are capable of regenerating from teristics. Within the succession process, there are changes in the their basal structure, making good use of the more favourable species composition that respond to the different requirements and conditions of increased nutrients and light that exist initially (Calvo competitive capacities of each species. In general, resprouting was A. Muñoz et al. / Journal of Environmental Management 94 (2012) 34e40 39 observed in all the shrub species present. The increase in the The conservation of the heathlands depends on their inclusion in biomass of the Ericaceae species that resprout after cutting is more natural conservation programmes and many authors have man- rapid and intense than after a half intensity fire (Casal et al., 1984). ifested the necessity for their recuperation using traditional uses, E. tetralix heathlands are characterised by a large number of such as cutting, burning, or grazing (Bardgett et al.,1995; Gimingham species, being one of the types of shrubland communities with et al., 1979; Hobbs and Gimingham, 1984). The cutting could be great species richness (Basanta et al., 1989). Cutting caused an considered as a useful tool for the sustainable management and increase of the number of species, above all in the first years, as was conservation of wet heathlands, of the endemic species of the found by Calvo et al. (2002a, 2002b). In this case it was the different stages, for controlling fire risk, to conserve their distinc- herbs species that increased in the first stages after cutting, as the tiveness and maintain the ecological, cultural, educational and social elimination of the vegetation canopy allowed the presence of value of these communities. The establishment of a mosaic of age different species such as the endemic Carex durieui. G. berberidea, classes with high heterogeneity is of great importance from the also endemic, is present in the late stages, for which a mosaic of conservation point of view (Calvo et al., 2007), since it increases the young and old classes favours the presence of both. Diversity values diversity of both vegetation and animals, revalorising the zone. found are quite high compared with other Galician shrublands, Compared to other alternative practices such as controlled burning, a characteristic already described by Basanta et al. (1988, 1989) and grazing or pulling-up, cutting is a low intensity disturbance that can they remain practically constant in all four stages. be incorporated in management plans, either alone or com- The structural variables of vegetation are to a certain point plemented with other practices. indicators of the degree of development of the community. This is According to Izco et al. (2006),theE. ciliaris and E. tetralix because the first stages of succession are characterised by both heathlands are the scarcest of Galicia, besides their being considered higher numbers of herbs species and by higher dominance. as the smallest in extent. This converts their management into Therefore, horizontal and vertical structures are profiled as the a priority. The inclusion of these communities in management plans indicators of the degree of succession, as it separates the stages is intended to achieve their valuation by the creation of a mosaic of quite clearly. age classes and the reduction of the availability of nutrients, through E. ciliaris and E. tetralix communities show great resilience to the sustainable management techniques such as mechanical cutting and cutting. The life forms or the diversity hardly vary between stages. elimination of biomass, or low-level burning. Following Symes and The structure changes over time after cutting, but the change is not Day (2003), the large areas of heathlands (more than 15e20 ha) large enough to be reflected in the diversity values. The succession can be divided into 1 ha patches, in such a way that a patch will be post cutting is an autosuccession, a recuperation of the spatial cut or burned each year until a cycle of 15 or 20 years is completed. structure that hardly affects the species composition and diversity. Also, smaller cycles could be considered, such as every 10 years, Cutting is an intervention that causes very little damage and the leaving areas intact that conserve the advanced stages. In the case of regenerated vegetation maintains its pre-existing composition communities with smaller areas (<5 ha), common in Galicia, it (Boivin, 1977; Casal et al., 1984; Pesqueira et al., 2005). This auto- would be better to create patches of 1 ha, cutting some patch every succession indicates a high resilience of the community. It has been 2e4 years to maintain different stages. If the area of the community observed in Cantabrian heathlands after cutting but also after is less than 1 ha, the whole of the surface will be cut every 10 years, burning (Calvoetal.,2002b;Jáureguietal.,2007). The dynamic which is the estimated time in which the community will reach succession after burning is widely documented in the heathlands of a mature structure. Calluna vulgaris. As stands of Calluna increase in age, they pass Finally, it is also necessary to take into account other factors of through four phases (pioneer, building, mature and degenerate) alteration, such as nearby industrial and agricultural-livestock which are quite easily recognised (Barclay-Estrup and Gimingham, activities, because they contribute to the contamination of the air 1969; Barclay-Estrup, 1970). The communities of Calluna have and the eutrophyzation of the subterranean waters. There are a high cultural and grazing value. After 10e15 years the number of numerous studies that demonstrate that the enrichment of N and P green shoots decrease considerably and so this is the best moment in the soil produces changes in the composition of the heathland for burning, promoting the regeneration of the community. (Aerts et al., 1990; Mitchell et al., 2000). For this reason it is of great Controlled burning hardly damages the plant buds and after three importance to control these activities in the areas to be conserved, years an almost complete recuperation of the cover exists. If the because if the nutrients are not removed from the ecosystem intervention cycle is of more than 15 years, the entrance of species through traditional usage it is possible that more rapid manage- that are not normally in the initial stages is permitted, principally ment techniques may have to be used at a later stage to maintain trees (Gimingham et al., 1979). In the case of E. ciliaris and E. tetralix the stability of the heathland and avoid the invasion of herbs or tree wet heathlands, with wet soils, where the most abundant species of species. the community are rhizomatous species; half-level burning that penetrates little into the soil allows regeneration (Schimmel and 5. Conclusions Granström, 1996). Studies made in Galicia (Muñoz, 2009)confirm this and show that half-level burning is adequate for the current The succession after cutting is an autosuccession, with gradual management of these heathlands, providing that it is carried out in differences between stages. The number of herbs species is higher the correct season and under controlled conditions (Bond and in the first stages after cutting and decreases as the succession Wilgen, 1996). With the future climate change (Solomon et al., advances, whilst woody vegetation predominates afterwards. 2007), the E. ciliaris and E. tetralix heathlands will tend towards Cutting does not produce significant changes in the measure- a lesser degree of summer swamping and the phreatic layer will ments of diversity. The vertical and horizontal structure reflects descend, drying and modifying the species composition of the the high degree of resilience of the plant community to this community, decreasing the number of specialist species in favour of practice and the multivariate analyses applied to the cover and generalist species and, thus, these ecosystems will lose their structural data of the shrubland shows that there are gradual ecological identity. Moreover, wildfires will be more frequent and differences between stages. Cutting represents a useful tool from more severe and will gravely affect the vegetation, the soil and the the heathland management point of view and should be used to microclimatic and hydrological features, making the recuperation of create a mosaic of vegetation with different succession stages and the wet heathlands very difficult. structures. 40 A. Muñoz et al. / Journal of Environmental Management 94 (2012) 34e40

Acknowledgements Gimingham, C.H., 1972. Ecology of Heathlands. Chapman and Hall, UK. Gimingham, C.H., Smidt, J.T., 1983. Heaths as natural and semi-natural vegetation. In: Holzner, W., Werger, M.J.A., Ikusima, I. (Eds.), Man’s impact on vegetation. We would like to thank E. Díaz-Vizcaíno and M. Basanta for their Dr. W. Junk, The Hague, The Netherlands, pp. 185e199. help in carrying out this study. During this study Ana Muñoz Gimingham, C.H., Chapman, S.B., Webb, N.R., 1979. European heathlands. In: received a Pre-Doctoral Grant from the Xunta de Galicia. The study Specht, R.L. (Ed.), Heathlands and Related Shrublands. Descriptive Studies. fi e “ ” Elsevier Scienti c Publishing Company, Amsterdam, pp. 361 413. was carried out within the projects PGIDIT02RFO20001PR , Godron, M., Daget, P., Long, G., Sauvage, Ch., Emberger, L., Le Flock, E., Poissonet, J., “PGIDT00MAM20001PR” and “PGIDIT07MRU006291PR”, all Wacquant, J.P., 1968. Code pour le relevé méthodique de la végétation et du financed by the Xunta de Galicia. milieu. CNRS, Paris. Grime, J.P., 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86, 902e910. Appendix. Supplementary material Hobbs, R.J., Gimingham, C.H., 1984. Studies on fire in Scottish heathland communities. I. Fire characteristics. J. Ecol. 72, 223e240. Izco, J., Amigo, J., Ramil-Rego, P., Díaz, R., Sánchez, J.M., 2006. Brezales: bio- Supplementary materials associated with this article can be diversidad, usos y conservación. Recursos Naturais 2, 5e24. found, in the online version, at doi:10.1016/j.jenvman.2011.08.006. Jáuregui, B.M., Celaya, R., García, U., Osoro, K., 2007. Vegetation dynamics in burnt heather-gorse shrublands under different grazing management with sheep and goats. Agroforest. Syst. 70, 103e111. References Jones, B., Molenda, O., Hayward, C., D’Aguiar, M., Miller, N., Rye, L., Cottenie, K., 2011. Patterns of tree diversity in response to logging in Algonquin Provincial Park. Aerts, R., Berendse, F., de Caluwe, H., Schmitz, M., 1990. Competition in heathland SURG 4, 56e62. along an experimental gradient of nutrient availability. Oikos 57, 310e318. Liley, D., 2005. Cutting of lowland heathland using a double-chop forage harvester Barclay-Estrup, P., 1970. The description and interpretation of cyclical processes in at Trigon, Dorset, England. Conserv. Evid. 2, 113e114. a heath community. II. Change in biomass and shoot production during the Marey, M.F., Rodríguez, V., Crecente, R., 2006. Using GIS to measure changes in the Calluna cycle. J. Ecol. 58, 243e249. temporal and spatial dynamics of forestland: experiences from north-west Barclay-Estrup, P., Gimingham, C.H., 1969. The description and interpretation of Spain. Forestry 3, 1e15. cyclical processes in a heath community. I. Vegetational change in relation to Mitchell, R.J., Auld, M.H.D., Hughes, J.M., Marrs, R.H., 2000. Estimates of nutrient the Calluna cycle. J. Ecol. 57, 737e758. removal during heathland restoration on sucessional sites in Dorset, southern Bardgett, R.D., Marsden, J.H., Howard, D.C., Hossell, J.E., 1995. The extent and England. Biol. Conserv 95, 233e246. condition of heather in moorland and the potential impact of climate change. Muñoz, A., 2009. Estructura y dinámica de comunidades de Erica ciliaris y Erica In: Thompson, D.B.A., Hester, A.J., Usher, M.B. (Eds.), Heaths and Moorland: tetralix en el marco de la gestión sostenible. Doctoral thesis. Universidad de Cultural Landscapes. HMSO, Edinburgh, pp. 43e50. Santiago de Compostela. Basanta, M., Díaz Vizcaíno, E., Casal, M., 1988. Structure of shrubland communities Ninyerola, M., Pons, X., Roure, J.M., 2005. Atlas climático digital de la Península in Galicia (NW Spain). In: During, H.J., Werger, M.J.A., Willems, J.H. (Eds.), Ibérica. Metodología y aplicaciones en bioclimatología y geobotánica. Uni- Diversity and Patterns in Plant Communities. SPB Academic Publishing, The versidad Autónoma de Barcelona, Bellaterra, Spain. Hague, The Netherlands, pp. 25e36. Oostermeijer, J.G.B., Vant’t Veer, R., Den Nijs, J.C.M., 1994. Population structure of the Basanta, M., Díaz-Vizcaíno, E., Casal, M., Morey, M., 1989. Diversity measurements in rare, long lived perennial Gentiana pneumonanthe in relation to vegetation and shrubland communities of Galicia (NW Spain). Vegetatio 82, 105e112. management in the Netherlands. J. Appl. Ecol. 31, 428e438. Boivin, J., 1977. Régénération aprés coupes mécanisées et conventionnelles: Cote- Pesqueira, X.M., Muñoz, A., Álvarez, R., García-Duro, J., Reyes, O., Basanta, M., Nord du Québec. For. Chron. 53, 341e347. Casal, M., 2005. Estudio ecológico del matorral atlántico de interés para la Bond, W.J., Wilgen, B.W., 1996. Fire and Plants. Chapman & Hall, London, UK. conservación. Respuesta estructural a usos tradicionales en Galicia. Rev. R. Acad. Calvo, L., Tárrega, R., De Luis, E., 2002a. Regeneration patterns in a Calluna vulgaris Gal. Cien XXIV, 41e60. heathland in the Cantabrian mountains (NW Spain): effects of burning, cutting Puentes, A., Basanta, M., 2002. Architecture of Ulex europaeus: changes in the and ploughing. Acta Oecol. 23, 81e90. vertical distribution of organs in relation to plant height and season. J. Veg. Sci. Calvo, L., Tárrega, R., De Luis, E., 2002b. Secondary succession after perturbations in 13, 793e802. a shrubland community. Acta Oecol. 23, 393e404. Rodríguez Oubiña, J., 1987. Estudio fitosociológico de las brañas de la provincia de A Calvo, L., Alonso, I., Fernández, A.J., De Luis, E., 2005. Short-term study of effects of Coruña. PhD thesis. Universidad de Santiago de Compostela, Spain. fertilisation and cutting treatments on the vegetation dynamics of mountains Schimmel, J., Granström, A., 1996. Fire severity and vegetation response in the heathlands in Spain. Plant Ecol. 179, 181e191. boreal Swedish forest. Ecology 77 (5), 1436e1450. Calvo, L., Alonso, I., Marcos, E., De Luis, E., 2007. Effects of cutting and nitrogen Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., deposition on biodiversity in Cantabrian heathlands. Appl. Veg. Sci. 10, 43e52. Miller, H.L., 2007. Contribution of Working Group I to the Fourth Assessment Casal, M., Basanta, M., García Novo, F., 1984. La regeneración de los montes Report of the Intergovernmental Panel on Climate Change. Cambridge Univer- incendiados en Galicia. Monografía No 99. Universidad de Santiago de Com- sity Press, Cambridge, United Kingdom and New York, NY, USA. postela, Spain. Symes, N.C., Day, J., 2003. A Practical Guide to the Restoration and Management of Celaya, R., Martínez, A., Osoro, K., 2007. Vegetation dynamics in Cantabrian Lowland Heathland. The RSPB, Sandy. heathlands associated with improved pasture areas under single or mixed Warren, M.S., Hill, J.K., Thomas, J.A., Asher, J., Fox, R., Huntley, B., Roy, B., Telfer, M.G., grazing by sheep and goats. Small Rumin. Res. 72, 165e177. Jeffcoate, S., Harding, P., Jeffcoate, G., Willis, S.G., Greatorex-Davies, J.N., Colombaroli, D., Tinner, W., Van Leeuwen, J., Noti, R., Vescovi, E., Vannière, B., Moss, D., Thomas, C.D., 2001. Rapid responses of British butterflies to opposing Magny, M., Schmidt, R., Bugmann, H., 2009. Response of broadleaved evergreen forces of climate and habitat change. Nature 414, 65e69. Mediterranean forest vegetation to fire disturbance during the Holocene: Webb, N.R., 1998. The traditional management of European heathlands. J. Appl. Ecol. insights from the peri-Adriatic region. J. Biogeogr. 36, 314e326. 35, 987e990. Ewing, S.A., Southard, R.J., Macalady, J.L., Hartshorn, A.S., Johnson, M.J., 2007. Soil Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., microbial fingerprints, carbon, and nitrogen in a Mojave Desert creosote bush Cavender-Bares, J., Chapin, T., Cornelissen, J.H., Diemer, M., Flexas, J., ecosystem. Soil Sci. Soc. Am. J. 71, 469e475. Garnier, E., Groom, P.K., Gulias, J., Hikosaka, K., Lamont, B.B., Lee, T., Lee, W., Garnier, E., Cortéz, J., Billés, G., Navas, M.L., Roumet, C., Debussche, M., Laurent, G., Lusk, C., Midgley, J.J., Navas, M.L., Niinemets, U., Oleksyn, J., Osada, N., Blanchard, A., Aubry, D., Bellmann, A., Neill, C., Toussaint, J.-P., 2004. Plant Poorter, H., Poot, P., Prior, L., Pyankov, V.I., Roumet, C., Thomas, S.C., functional markers capture ecosystem properties during secondary succession. Tjoelker, M.G., Veneklaas, E.J., Villar, R., 2004. The worldwide leaf economics Ecology 85 (9), 2630e2637. spectrum. Nature 428, 821e827.