Biological Conservation 126 (2005) 234–246 www.elsevier.com/locate/biocon

ButterXies highlight the conservation value of hay meadows highly threatened by land-use changes in a protected Mediterranean area

Constantí Stefanescu a,¤, Josep Peñuelas b, Iolanda Filella b

a ButterXy Monitoring Scheme, Museu de Granollers Ciències Naturals, Francesc Macià, 51, E-08400 Granollers, b Unitat EcoWsiologia CSIC-CEAB-CREAF, CREAF (Centre for Ecological Research and Forestry Applications), EdiWci C, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain

Received 18 February 2005; received in revised form 17 May 2005; accepted 20 May 2005 Available online 19 July 2005

Abstract

ButterXy assemblages were used to characterize and evaluate the conservation value of the main habitat types in the Aiguamolls de l’Empordà Natural Park (north-eastern Spain), an important protected wetland area on the Mediterranean coast. ButterXy data were obtained from a number of transects walked as part of the Catalan ButterXy Monitoring Scheme, which uses a standardized methodology for monitoring butterXies. A Mantel test indicated a strong association between habitat types and the composition of butterXy assemblages and a principal component analysis ordinated individual butterXy species along a gradient from woodland to open areas, thereby indicating various degrees of shade tolerance. In addition, cluster analysis distinguished two main groups of hab- itats based on the similarities of their butterXy fauna: woodland and bramble clumps and a group of three diVerent kinds of grass- lands (traditionally hay meadows, pastures, and alfalfa Welds). Hay meadows Xooded in winter (the so-called closes) appeared always as the highest ranked habitat in terms of conservation evaluation: they have more butterXies and a slight tendency to harbor more and generally rarer species. This conclusion coincides with that of previous investigations that have indicated that the most diverse and rare plant communities in the whole Natural Park are present in the closes, and highlights the importance of traditionally man- aged hay meadows for wildlife. However, these hay meadows – one of the rarest habitats in the Mediterranean region – are in alarm- ing decline and have become the most threatened habitat in this protected area: no longer proWtable, we believe that the future of the closes will depend ultimately on the existence of agri-environmental schemes.  2005 Elsevier Ltd. All rights reserved.

Keywords: ButterXies; Hay meadows; Conservation value; Life history; Mediterranean region

1. Introduction 1983 and has subsequently been included in the Ramsar list of Wetlands of International Importance. As well, it Situated on the shores of the Bahia de Roses, close to also harbors populations of several rare invertebrate the eastern tip of the Pyrenees, the Aiguamolls de l’Emp- taxa, especially those associated with wetland habitats ordà constitute one of the most important areas for (e.g., Pérez De-Gregorio, 1990). wildlife on the Mediterranean coastline of the Iberian The vegetation of the Aiguamolls de l’Empordà Nat- Peninsula. Traditionally, highly appreciated for its orni- ural Park (hereafter AENP) has also been studied in thological value (Sargatal and del Hoyo, 1989), this pro- detail and analyses of the plant diversity occurring in the tected area (4784 ha) was declared a Natural Park in area as a whole (Farràs and Velasco, 1994; Watt and Vilar, 1997; Gesti and Vilar, 1999) and the impact of * Corresponding author. Tel./fax: +34 93 870 96 51. management policies on plant communities (Gesti, 2000) E-mail address: [email protected] (C. Stefanescu). have been carried out. These studies have revealed the

0006-3207/$ - see front matter  2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.05.010 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 235 exceptional value of the so-called closes, one of the most 2000), a monitoring program based on the standard limited and threatened habitats in the Natural Park. methodology of the British ButterXy Monitoring Closes are meadows enclosed by drainage canals lined by Scheme (Pollard and Yates, 1993). The wealth of infor- riverine forest that Xood in winter and, depending on mation accumulated throughout these years now their production, are mowed for hay once or twice a enables us to assess the conservation value of various year. A recent analysis by Gesti et al. (2003) has shown habitats in the AENP by using butterXies as a bioindica- that the most typical plant community of the closes tor group. This is important in the context outlined (Arrhenatheretum elatioris Br.-Bl., 1915) has the highest above, as it allows us to rank the closes by means of an species richness and diversity of all plant communities independent data set provided by a well-studied and present in the area, and is also home to the region’s rar- highly valuable indicator taxa. Moreover, this additional est taxa (i.e., those with the most restricted distributions information seems especially pertinent in this case given in Catalonia, northeast Spain). Moreover, these authors that several works have shown a lack of correlation warn that this habitat is disappearing rapidly. In 1956, between butterXy and plant diversity (e.g., Stefanescu 136.04 ha of closes were present in the area, but by 2002 et al., 2004, using data from the CBMS) and butterXy this Wgure had dropped to just 26.75 ha as a result of and moth diversity (Ricketts et al., 2002) at the local agricultural improvement (e.g., conversion to the pro- scales considered in our study (0.1–10 km2). These poten- duction of maize, sunXower, and rice) and the gradual tial disagreements could lead to serious conXicts in the change from hay to fodder as the main food source for designation of the areas or habitats most worthy of the cattle. The problem still exists, despite the declaration of greatest conservation eVorts. the whole area as a Natural Park. In this paper, we use data from the butterXy monitor- Unfortunately, evidence of the importance of the ing transects in the AENP to address several questions closes for other taxa is at present somewhat lacking. of obvious conservation interest in a protected area. Stefanescu and Miralles (1994) studied moth assem- First, we ask if butterXy assemblages are distributed blages in three sites located at diVerent distances from homogeneously or heterogeneously across the diVerent the coastline corresponding to three well-deWned and habitat types of the Natural Park. In the latter case, it characteristic habitats of the AENP: a typical saltmarsh, may be possible to deWne regular associations of groups an extensive reed bed and a traditional closa. Their anal- of species in particular habitats and select subsets of spe- ysis, based on data obtained by light trapping in two cies that may be used as bioindicators of some particular consecutive years, revealed important diVerences in the environmental conditions. Secondly, once this question moth fauna of the three sites and showed that the closa has been answered, we assess the conservation value of site harbored the most diverse and species-rich moth each habitat type on the basis of its butterXy fauna. Our assemblage. The bird communities of several closes have results are compared with those from earlier botanical also been monitored in recent years (Montràs, 2004), studies that have highlighted the ecological importance mainly as a tool for understanding the phenological pat- of the closes. Underlying this comparison is the fact that tern of habitat use by diVerent species. However, this a coincidence in the results of both studies would pro- study does not compare the bird communities of the vide stronger arguments for an eVective protection of closes with those present in other habitats within the this threatened habitat. Finally, we also seek out correla- Natural Park. tions between habitat type and the diVerent life history The lack of comprehensive studies of any taxonomic attributes of the butterXy species present, which, as group other than higher plants undoubtedly represents recently shown, may have important implications for an obstacle when trying to protect the remaining closes conservation (Dennis et al., 2004). in the AENP. In fact, an increasing number of studies have shown a lack of agreement in cross-taxonomic pat- terns of species richness and endemism at scales of 2. Material and methods several orders of magnitude, including at the Wne-scale patterns considered here (e.g., Prendergast et al., 1993; 2.1. Transects and butterXy data Oliver et al., 1998; Vanjaarsveld et al., 1998; Kremen et al., 2004). Obviously, this is good reason to avoid the ButterXy data were obtained from six CBMS moni- former common practice of assessing the conservation toring transects (Stefanescu, 2000), all of which were value of wildlife areas using data from a single taxo- located within the AENP (Fig. 1). The transects were sit- nomic group. uated at various distances from the sea and provide a Apart from birds, butterXies stand out as the most representative sample of the main biotopes found in the intensively studied wildlife group in the AENP. Since Natural Park: a mosaic of grasslands (hay meadows, 1988 several monitoring transects have been operated in pastures and alfalfa Welds), rides delimited by woodland diVerent parts of the Natural Park as part of the Catalan (mainly riverine forest), bramble and helophytic vegeta- ButterXy Monitoring Scheme or CBMS (Stefanescu, tion, and arable Welds. 236 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246

Fig. 1. Map of the Aiguamolls de l’Empordà Natural Park, showing the location of the six CBMS transects that provided the butterXy data. Num- bers refer to the original codes of the transects in the CBMS: 1 – El Cortalet; 2 – La Rubina; 3 – Vilaüt; 22 – Closes de l’Ullal; 23 – Closes del Tec; 59: Mig de Dos Rius.

As per the standard methodology of the BMS (see clumps (0: absence; 1: 10–30%; 2: >30%); (v) absence Pollard and Yates, 1993, for details), recorders walked (0) or presence (1) of arable Welds at the sides of the Wxed routes and counted butterXies detected within 2.5 recording route. Data on the relative cover of vegetation m on either side of the route and up to 5 m ahead. types was extracted from the CBMS data base, which Counts were made on a weekly basis starting on March includes information on the percentage occupied by 1 and ending on September 26, a period of 30 recording plant communities within the 2.5 m-belt on each side of weeks per year. Transects were divided into discrete sec- the progression line of the transect routes, as character- tions, which coincided with obvious changes in vegeta- ized by a botanist in accordance with the CORINE tion type, and separate counts were made in each section. Biotopes Manual (Moss et al., 1990). Plant communities Five categorical variables were used to characterize the were characterized in the Wrst or second year of the mon- 46 sections included in this study: (i) relative cover of itoring of a transect; however, in El Cortalet, which has grasslands (0: <30% of the recording route; 1: >30%); (ii) been recorded for the whole period 1988–2004, vegeta- absence (0) or presence (1) of cattle grazing in grass- tion was characterized for a second time in 2000. A brief lands; (iii) relative cover of woodland (0: absence; 1: 10– deWnition of the 46 sections, together with the values of 30%; 2: >30%); (iv) relative cover of bramble hedges or each categorical variable, is given in Appendix A. C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 237

Because three of the six transects were only analyses were performed using the STATISTICA pack- monitored for one year (La Rubina, 1988; Vilaüt, age v. 5.0 for Windows (Statsoft, Inc., Tulsa, OK, USA). 1989; Closes de l’Ullal, 1996), in the other three tran- sects we also only used data from one recording season 2.4. Habitat types for butterXies: conservation value and to assess butterXy species abundance in each section. ecological characterization Data from Closes del Tec correspond to the Wrst year of monitoring (1997), when they were actively man- In order to detect the main habitat types that can be aged as hay meadows or pastures. For El Cortalet and characterized by consistent butterXy assemblages, a Mig de Dos Rius, we selected the year in which the cluster analysis was applied to the species abundance plant communities were characterized (2000 and 2002, matrix. We used the reduced data set given the limited respectively). Moreover, we also included data from ability of the rarest species to reveal clear patterns. 1988 for six sections in El Cortalet that, at that time, Thus, the Wnal input matrix consisted of 46 columns sampled habitats that are no longer present in the (sections) and 27 rows (butterXy species). Linkage dis- transect (e.g., dry pastures and arable Weld margins). tance was chosen as the similarity coeYcient and For each section, butterXy data were standardized as UPGMA as the clustering algorithm (e.g., Sneath and the individuals recorded in 100 m of transect through- Sokal, 1973). out the season. Each of the habitat types identiWed by the cluster analysis was characterized by several ecological param- 2.2. Correlation between butterXy assemblages and eters; diVerences between groups were analyzed using habitat types one-way ANOVA and LSD post hoc tests. Data were log transformed (or arc-sine transformed in the case of The existence of a correlation between habitat types proportions) whenever assumptions of normality and and the composition of butterXy assemblages was homoscedasticity were not met. For this ecological investigated using a Mantel test, which compares two characterization, we used the complete data set (i.e., similarity matrices computed for the same objects and comprising all 47 butterXy species appearing in the obtained independently of each other (Legendre and samples). Legendre, 1998). In our case, matrix Y contains similar- A Wrst set of parameters, selected because of their fre- ities between the sites (i.e., the 46 studied sections) in quent use as criteria for conservation evaluation, were terms of butterXy species composition, while matrix X chosen (e.g., Usher, 1986): (i) species richness, (ii) abun- contains similarities in environmental characteristics dance, and (iii) rarity. Two measures of species richness for the same sites (i.e., the scores of each of the Wve cat- were used: (a) all species recorded and (b) only those spe- egorical variables used to characterize each section) cies that were recorded with an abundance of >1 individ- listed in the same order. Calculations were made with ual/100 m of transect (i.e., excluding occasional or the program Mantel (250 permutations) from the “R” vagrant species). Abundance was deWned as the number package of multivariate analysis v. 3.0 (Alain Vauder, of butterXies recorded in 100 m of transect for all species University of Montreal, Quebec, Canada). A one-tailed combined. Rarity was measured at two diVerent spatial test was used to test for a positive correlation between scales: (a) within the Natural Park (i.e., local scale) as 1/ the two matrices. ni, where ni is the number of sections (out of a total of 46) where species i was recorded, and (b) within the CBMS 2.3. Indicator species (i.e., regional scale), again as 1/ni, where ni is the number of CBMS transects in Mediterranean habitats (out of a Species matrices were analyzed by ordination using total of 54) where species i was recorded. Thus, in the principal component analysis (PCA) to identify sets of Wrst case values ranged from 0.022 to 1, and in the sec- species characterizing the main habitat types in a reduced ond case from 0.019 to 1. Higher values corresponded to dimensional space. As input, data for both butterXy pres- rarer species. ence–absence and abundance adjusted for transect We also selected a second set of parameters that are length, together with the habitat type variables, were widely used in studies aiming to relate life-cycle used. Both analyses were performed on the complete data strategies to habitat characteristics (i.e., habitat perma- set (all 47 species observed) and for a reduced data set nence, habitat complexity, and resource diversity and comprising only 27 of the “commonest species” (arbi- availability; Brown, 1985; SteVan-Dewenter and trarily deWned as those appearing with an abundance of Tscharntke, 1997; Dennis et al., 2004): (i) body size, (ii) at least one individual/100 m of transect in at least three overwintering stage, (iii) generations per year or voltin- sections). Although similar results were produced for ism, (iv) host-plant specialization, and (v) dispersal abil- both cases, we present here only the results obtained with ity. Body size was estimated as the mean forewing length the quantitatively reduced data set (abundance data for of males (data from Higgins and Riley, 1984). We calcu- the 27 “commonest” species). This and all subsequent lated for each habitat type the relative contribution 238 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246

(i.e., the proportion) of (a) species overwintering as 1 egg, , pupa, adult, or unable to overwinter (i.e., Ov migrant species), (b) species having one (univoltine), Pym Ml Lp Va two (bivoltine), or three or more (multivoltine) genera- Pya tions per year, and (c) species feeding as larvae on a 0.5 Pb Ca Lph Pc Woodland Car Pt Ii single host-plant genus (monophagous), on several Pn Pa Lb Pm genera within a single plant family (oligophagous), or Pr Lm Bramble hedge Ac on several genera belonging to a number of plant fami- Mj Pla lies (polyphagous). Biological data were obtained from 0 Arable field Cp Grassland Cca Pce Pi Cc Tolman and Lewington (1997) and from personal Factor 2 observations from within the study area. Finally, an Cattle grazing overall index of dispersal ability was calculated after classifying each species into one of the following Wve -0.5 categories: 0 – forming closed populations with very little dispersal; 1 – closed populations with more fre- quent dispersal; 2 – closed populations with common dispersal; 3 – open populations with non-directional -1 -1 -0.5 0 0.5 1 dispersal; 4 – open populations with directional migra- Factor 1 tion. Data on dispersal ability and population structure were obtained from various sources (e.g., Pollard and Fig. 2. ButterXy species and habitat variable distribution as a function W Eversham, 1995; Dennis and Shreeve, 1996; personal of the two rst principal axes in the PCA analysis conducted on the matrix of correlations between the depicted variables. Abbreviations observations). The ecological attributes for the 47 for species: Ac, Aricia cramera; Ca, Carcharodus alceae; Car, Celas- butterXy species detected in our samples are summarized trina argiolus; Cp, Coenonympha pamphilus; Cc, Colias crocea; Cca, in Appendix B. Cynthia cardui; Ii, Inachis io; Lb, Lampides boeticus; Lm, Lasiommata megera; Lp, Leptotes pirithous; Lph, Lycaena phlaeas; Mj, Maniola jur- tina; Ml, lachesis; Ov, Ochlodes venata; Pm, Papilio mach- aon; Pa, Pararge aegeria; Pla, Plebejus argus; Pb, Pieris brassicae; Pn, 3. Results Pieris napi; Pr, Pieris rapae; Pc, Polygonia c-album; Pi, Polyommatus icarus; Pya, armoricanus; Pym, Pyrgus malvoides; Pce, 3.1. ButterXies as indicators of habitat types cecilia; Pt, Pyronia tithonus; and Va, Vanessa atalanta.

The Mantel test (r D 0.61, p D 0.003) indicated that the similarity matrices of butterXy composition and habitat erence towards each habitat type. Pararge aegeria, types are strongly correlated. Therefore, a certain combi- Pieris napi, Celastrina argiolus and Polygonia c-album nation of vegetation units in our transect sections (i.e., were the most characteristic species of woodland and the relative cover of grassland, bramble hedges or wood- bramble hedges and represent the most shade-tolerant land along the transects) translates into a highly charac- butterXies in our study. At the opposite end of the teristic butterXy assemblage. axis, Colias crocea, Polyommatus icarus and Coen- The nature of this close association was further onympha pamphilus appeared strongly associated with studied by means of a PCA applied to the original grasslands; that is, they are typically found in the matrices of butterXy abundance and habitat types. A most open conditions. The PCA did not show a clear 35.2% of variation in the data was accounted for by the diVerentiation within each of the two extreme situa- Wrst two axes in the new reduced multidimensional tions, i.e., no butterXy species appeared to prefer space (Fig. 2). The Wrst axis (19.3% of variation) had a woodland to bramble hedges or hay meadows over clear biological meaning and could be interpreted as a pastures. gradient between sections dominated by woodland and This ordination also suggested that several species bramble (negative values) and sections mainly consist- with relatively low positive values (e.g., Maniola jurtina, ing of grasslands (both hay meadows and pastures; Pyrgus malvoides, Ochlodes venata, Melanargia lachesis, positive values). The position of arable Welds near and Pyronia cecilia) or relatively low negative values woodland and bramble clumps is explained by the (e.g., Pyronia tithonus and Lasiommata megera) prefer coincidence of these three kinds of habitats wherever habitats with intermediate characteristics of grasslands intensive farmland was sampled; for practical reasons and woodland. the transect routes ran along the edges of arable Welds, which mainly consisted of riverine forest or bramble 3.2. Major butterXy habitats patches. The 27 commonest butterXy species were also ordi- The cluster analysis allowed us to distinguish two nated along the Wrst axis, showing their relative pref- main groups of habitats based on the similarities C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 239

Fig. 3. Dendrogram based on the cluster analysis of 46 transect sections and 27 butterXy species. The between-samples measurement of similarity was ‘Linkage distance’, and the clustering algorithm was UPGMA. Main groupings of sections: A, woodland habitats; B, grassland habitats. The corre- spondences of further subdivisions of the two main groups to particular habitats (A1, A2, B1, B2, B3) are given below each cluster. within the butterXy assemblages that live there 3.3. Comparison of butterXy habitats (Fig. 3). In accordance with the PCA results, the Wrst group (A) consisted of those sections dominated by The mean values (§SE) of the selected ecological woodland, by bramble clumps replacing former parameters in the diVerent groups are shown in Figs. 4 woodland, or both. The second group (B) corre- and 5. sponded to those sections that sampled a diversity of grasslands. However, further subgroups were evident 3.3.1. Criteria for conservation evaluation within each main class, indicating a Wner association Of those criteria most often employed for conserva- between butterXy assemblages and the habitats occur- tion evaluation, we only found signiWcant diVerences in ring along the transects. In particular, we considered butterXy abundances (log individuals/100 m of transect: the Wve following major butterXy habitats (as deWned F D 4.08, p < 0.01). ButterXies were more abundant in tra- from the cluster analysis when the linkage distance is ditional hay meadows than in any other of the habitat set at around 0.5, Fig. 3), which represent useful eco- types; few diVerences were detected within these other logical units: habitat types (Fig. 4(a)). Hay meadows also ranked Wrst for species richness, • Subgroup A1: rides and arable Weld edges delimited independently of which of the two sets of species was by woodland, mainly elms (Ulmus minor), ashes used, while woodland was determined as the most spe- (Fraxinus oxycarpa), and oaks (Quercus humilis), or cies poor habitat (Fig. 4(b)), although overall no signiW- bramble (Rubus umilfolius and R. caesius). cant diVerences were found between habitats. • Subgroup A2: open woodland interspersed with small Marginal signiWcant diVerences between groups were grassy patches, and woodland-grassland ecotone. also found for one of the two criteria of rarity used in • Subgroup B1: traditional hay meadows. this study (rarity at the regional scale: F D 2.21; p <0.1; • Subgroup B2: alfalfa Welds, harvested 2–3 times a Fig. 4(c)). Hay meadows were again ranked as the most year. valued habitat (e.g., the one having the rarest species), • Subgroup B3: pastures or hay meadows also used for with almost the same value as pastures. SigniWcant diVer- grazing. ences were only found between pastures and woodland, which harbored the commonest butterXy species. Similar These units, which correspond to truly discernible results were obtained when rarity was deWned on a local broad habitat types, are characterized by means of their scale. Both measures of rarity were highly correlated butterXy fauna below. (r D 0.55, p <0.001, n D 42). 240 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246

p D 0.07; Fig. 5(b)–(d)). Finally, dispersal ability was a 2.6 higher in alfalfa Welds and woodland than in pastures b 2.4 (F D 3.95; p D 0.009; Fig. 5(f)). On the other hand, diVerences in host-plant specialization and voltinism 2.2 were almost non-existent (with the exception of a likely a a a higher proportion of bivoltine species in hay meadows 2 a and pastures: F D 2.48; p D 0.06; Fig. 5(e)).

Abundance 1.8

(log individuals/100 m) 1.6 4. Discussion

1.4 X b Butter ies have traditionally been viewed as an excel- lent group of bioindicators, mainly due to the complex- 1.2 ity of ecological management required by many species (Thomas, 1991; New et al., 1995) and, more recently, to 1 their great ability to act as indicators of climate change (Parmesan, 2003). Accordingly, several monitoring methods have been developed to provide detailed data 0.8 on butterXy numbers and phenology. Species richnes One methodology that has proved particularly use- (log number of species) 0.6 ful for monitoring butterXies in temperate countries is the so-called ButterXy Monitoring Scheme or BMS -1.5 c (Pollard and Yates, 1993). Reliable data on butterXy abundance and local distribution, as well as the eVects of managing practices on butterXy populations, can be -1.55 easily obtained by means of repeated visual censuses ) i along a transect route. One advantage of the BMS is the fact that the transect route is divided into a diVer- Rarity

(log 1/n b ent number of sections, coinciding with obvious -1.6 ab changes in the vegetation, and thus provides Wner scale ab data that can be used to assess biotope aYliations for a ab butterXy species (e.g., Oostermeijer and van Swaay, -1.65 1998). Indeed, as shown by Shreeve et al. (2001), not A1 A2 B1 B2 B3 only the requirements for precise larval host plants but Woodlands Grasslands also for other resources such as the hibernation site, adult feeding nectar sources, mate-locating locations, Fig. 4. Mean values (§SE) of three conservation evaluation criteria for diVerent habitats according to their butterXy fauna. (a) Abundance of and basking sites have led, in many cases, to close asso- butterXies, (b) species richness (occasional species excluded), and (c) ciations of diVerent groups of species or assemblages rarity (at the regional scale: 1/ni, where ni is the number of CBMS tran- with particular habitats or biotopes. This makes it pos- sects from a total of 54 where species i was recorded). See Fig. 3 for the sible to assess the conservation value of diVerent habi- W V W V de nition of habitat types. Di erent letters refer to signi cant di er- tat types on the basis of their characteristic butterXy ences (p < 0.05, LSD post hoc tests) among groups. fauna. In this study, data from the CBMS from six transects located in a Mediterranean Natural Park were used for 3.3.2. Life-history attributes this purpose. Data on butterXy abundance and vegeta- Changes in the composition of butterXy assemblages tion characteristics from a total of 46 transect sections resulted in notable diVerences in some basic life-history clearly indicated the existence of a strong association attributes of the species (Fig. 5). ButterXy species tended between butterXy assemblages and habitat type. This to be smaller in hay meadows and pastures than in relationship was further examined by PCA and cluster woodland (wing length: F D 2.69; p D 0.046; Fig. 5(a)). In analysis to reveal preferences of individual species and addition, overwintering strategies clearly diVered characteristic butterXy assemblages. between woodlands and grasslands. Relatively more spe- Individual species were ordinated along an axis repre- cies overwintered as larvae in open habitats than in for- senting a gradient from woodland (riverine forest and ested habitats (F D 6.17; p < 0.001), and the opposite was dense bramble clumps) to open areas (grasslands). Most true for species overwintering as pupae (F D 5.47; of the species occupied intermediate positions along the p < 0.01) and, almost signiWcantly, for adults (F D 2.36; positive side of this axis, suggesting a preference for C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 241

a d 24 b b 15 a ab 22 ab b b 10 ab 20 ab

(arcs in) a Body size 18 5 Overwintering as adult (winglength in mm) 16 0 55 b e c 25 b bc 50 bc b ab 20 ab a ab 45 a 15 (arc sin)

40 (arc sin) Bivoltine 10

35 5 Overwintering as larva

30 0

c f 36 c b 2.6 b b bc abc 32 ab ab 2.4 a a 28 2.2 (arc sin) 2 24 Dispersal ability Overwintering as pupae 1.8 20 A1 A2 B1 B2 B3 A1 A2 B1 B2 B3 Woodlands Grasslands Woodlands Grasslands

Fig. 5. Mean values (§SE) of six life-history attributes of butterXy species in Wve diVerent habitats. (a) Body size, (b) proportion of species overwin- tering as larvae, (c) proportion of species overwintering as pupae, (d) proportion of species overwintering as adults; (e) proportion of bivoltine spe- cies, and (f) dispersal ability. DiVerent letters refer to signiWcant diVerences (p < 0.05, LSD post hoc tests) among groups. See the text for more details and Fig. 3 for the deWnition of habitat types. open habitats with some presence of patches of wood- characteristic grassland species in our data. At the other land or shrubs. The most likely explanation for this Wnd- extreme, P. aegeria and P. napi appeared as the most ing is the need butterXies have for elements providing typical examples of woodland butterXies in our study shelter and certain other resources (e.g., sites for perch- and as the most shade-tolerant species in English ing males or protected egg-laying sites; see Dover et al., woodlands. An important issue to investigate further 1997; Ouin and Burel, 2002), as well as their general pref- is how habitat preference of individual species varies erence for open areas. Moreover, a predictable decrease across large geographical areas; that is, how their bioin- in many butterXy populations and, eventually, a loss of dicator properties change or remain constant under diversity occurs whenever these elements increasing diVerent environmental conditions (e.g., Thomas, 1993; landscape complexity are removed, as is currently occur- Thomas et al., 1998). In this respect, the availability of ring in farmland (van Swaay and Warren, 1999). BMS data from several European countries is essential Our results also bear some resemblance to those of and may help to predict trends in species that can be Warren (1985) and Greatorex-Davies et al. (1993), who linked to widespread land-use changes in each country. deWned a gradient of shade tolerance for butterXies From the perspective of butterXy assemblages, cluster occurring in English woodlands. For instance, C. pam- analysis clearly distinguished between two broad habitat philus and P. icarus appeared at the extreme end of types, i.e., those sections corresponding to basically open shade intolerance in the studies of Warren (1985) and areas and those sections dominated by woodland. These Greatorex-Davies et al. (1993), and also as the most categories could be further divided into several butterXy 242 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 habitats (Fig. 3), depending on more subtle characteristics (competitive, stress-tolerant, and ruderal) to butterXy related to vegetation and management practices (e.g., tra- biology, and found signiWcant correlations between some ditional hay meadows, pastures, and alfalfa Welds were butterXy biological traits and host-plant strategies. For separated as distinct grassland habitats). A key aspect of example, they predicted an increase in wing surface-area, the present study was the assessment of the conservation mobility, and adult overwintering in butterXies associated value of these habitats and, more particularly, of hay with woodlands, and the opposite in butterXies living in meadows for butterXies. Interestingly, although signiWcant meadows, as indeed occurred in our study. They also pre- diVerences were only found for one (on a signiWcance level dicted an increase in larval overwintering and conserva- of p< 0.05) or two (on a signiWcance level of p< 0.1) of the tion status in butterXies associated with meadows, again three selected criteria (abundance, species richness, and just as we found in our study. On the other hand, some rarity), traditional hay meadows always appeared as the other predictions failed, especially those relating host- highest valued habitat: they contain more butterXies and, plant specialization and voltinism to host-plant strate- as well, show a slight tendency to harbor more and gener- gies. Although with our limited data it is not possible to ally rarer species. At the other extreme, woodland was fully evaluate the applicability of Dennis et al.’s predic- generally ranked as the least valuable habitat. tions, we believe that the coincidences are encouraging Our conclusion broadly coincides with that of Gesti and deserve further investigation with broader data sets. et al. (2003), who based their assessment of the conserva- tion value of hay meadows on higher plants. It has to be said, however, whereas these authors found a notably 5. Conclusion greater species richness amongst higher plants in hay meadows than in other habitats, in our study this trend The so-called closes, one of the most characteristic hab- could only be suggested. In any case, this discordance is itats in this Spanish Natural Park (AENP), were ranked not surprising considering the lack of a general corre- Wrst in the conservation evaluation of several habitat types lated pattern between butterXy and plant species rich- using butterXies as a bioindicator taxon: the same result ness (e.g., Kremen, 1992; Hawkins and Porter, 2003; was obtained when higher plants were employed as the Stefanescu et al., 2004). Most probably, the high abun- selected bioindicator taxon. Thus, these two Wndings high- dance of butterXies in these hay meadows can be light the importance for wildlife of these traditionally explained in terms of the high nectar supply (C. Stefane- managed hay meadows. This fact, together with the scu, unpublished data) and the abundance of key larval alarming decrease in extension of the closes in the AENP host plants (e.g., various Leguminoseae used by Lycae- and the rarity of this kind of habitat in the Mediterranean nids) in comparison to woodland habitats and, to a region, lead us to consider them as the most threatened lesser extent, grazed meadows. and one of the most valued habitats in this protected area. Apart from diVerences in the conservation value of Paradoxically, the declaration of the area as a Natu- habitats, our study also revealed striking diVerences in ral Park has not prevented the loss of the closes and has some basic life-history attributes in the butterXy assem- even accelerated the process. Thus, it has been estimated blages. For instance, it was clear that the butterXies of that 80% of the closes have been lost over the last 50 hay meadows and pastures tended to be smaller and have years, and that at least 60% have disappeared since the a poorer dispersal ability than those of woodland and area became legally protected in 1983 (Gesti et al., 2003). alfalfa Welds. In addition, relatively more butterXies over- There are two main reasons to explain this apparent wintered as larvae in all types of grasslands, while there anomaly. Firstly, most of the protected land is in private was a tendency for species to overwinter as pupae or hands (a common situation in many Spanish Natural adults in woodland. These diVerences can be accounted Parks), which hinders proper management based on the for, albeit only partially, by some basic features of the application of wildlife conservation criteria. Secondly, habitats, as suggested in the seminal works by South- the traditional management of grasslands (e.g., as hay wood (1962, 1977). Thus, the greater dispersal ability of meadows or pastures) is no longer proWtable, which butterXies in alfalfa Welds as opposed to that of the other eventually leads to the abandoning of these practices in two grassland habitats can be explained in terms of their the absence of any eVective Wnancial support. lower habitat permanence (these Welds are harvested We believe that the future of this and other grassland three or even more times per season). On the other hand, habitats in the Mediterranean will ultimately depend on the greater dispersal ability of butterXies in woodland, the existence of agri-environmental schemes such as those which corresponds to a late successional and more stable already operating in countries in northern Europe (e.g., and competitive habitat, contradicts the above argument. Ovenden et al., 1998). If this does not occur, then these Instead, this and other traits are better explained by host- man-managed habitats together with their exceptionally plant strategies, as recently suggested by Dennis et al. rich wildlife will soon disappear as just another example (2004). These authors linked the three-strategy system of a general trend aVecting the whole Mediterranean developed by Grime (1974) to explain plant strategies region (Bacaria et al., 1999; Blondel and Aronson, 1999). C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 243

Acknowledgements the English version. This research was partly supported by Grants REN2003–04871 and CGL2004-01402/BOS from Josep Espigulé, Francesc Giró, Lluc Julià, Eduard the Spanish Government, and European project ALARM Marquès, Marta Miralles, Sergi Romero, and Jordi Sarga- (Contract 506675, EU sixth framework program). The tal have given their support to the CBMS in Aiguamolls ButterXy Monitoring Scheme in Catalonia is funded by de l’Empordà Natural Park. Data on vegetation were pro- the Departament de Medi Ambient i Habitatge de la Gener- vided by Cèsar Gutiérrez and Susan Watt. Ferran Páramo alitat de Catalunya. The Fundació Territori i Paisatge has kindly prepared the map, and Michael Lockwood revised also given Wnancial support to this project.

Appendix A

Description of the 46 transect sections together with the values for each vegetation category variable Section label Habitat description Categorical habitat variables Grassland Cattle Woodland Bramble Arable cover grazing cover cover Weld Cort-1-00 Open woodland ride 0 0 1 1 0 Cort-2-88 Dry pasture 1 1 0 0 0 Cort-3-88 Dry pasture 1 1 0 0 0 Cort-4-00 Woodland ride 0 0 2 1 0 Cort-7-88 Track delimited by rice Welds and riverine forest 0 0 1 1 1 Cort-9-00 Hay meadow also used for grazing 1 1 0 0 0 Cort-10-00 Woodland ride 1 0 1 1 0 Cort-11-00 Hay meadow also used for grazing 1 1 0 1 0 Cort-11-88 Maize Weld edge 0 0 1 1 1 Cort-12-00 Woodland-hay meadow ecotone 1 0 1 1 0 Cort-12-88 Maize Weld edge 0 0 1 1 1 Cort-13-00 Woodland-hay meadow ecotone 1 0 1 1 0 Cort-13-88 Maize Weld edge 0 0 1 1 1 Cort-14-00 Woodland ride 0 0 1 1 0 Cort-15-00 Sun-Xower Weld edge 0 0 0 1 1 Mig-1-02 Hay meadow 1 0 0 0 0 Mig-2-02 Hay meadow 1 0 0 0 0 Mig-4-02 Woodland-hay meadow ecotone 1 0 2 1 0 Mig-5-02 Open woodland ride 1 0 2 1 0 Rub-1-88 Track delimited by helophytic vegetation 0 0 0 1 0 Rub-2-88 Track delimited by helophytic vegetation 0 0 0 1 0 Rub-4-88 Alfalfa Weld 1 0 0 1 0 Rub-7-88 Track delimited by helophytic vegetation 0 0 0 1 0 Rub-8-88 Alfalfa Weld 1 0 0 1 0 Rub-9-88 Hay meadow 1 0 0 1 0 Rub-10-88 Alfalfa Weld 1 0 0 1 0 Rub-11-88 Alfalfa Weld 1 0 0 1 0 Rub-12-88 Alfalfa Weld also used for grazing 1 1 0 1 0 Tec-1-97 Hay meadow 1 0 1 1 0 Tec-2-97 Hay meadow also used for grazing 1 0 0 1 0 Tec-3-97 Hay meadow also used for grazing 1 1 0 0 0 Tec-4-97 Woodland-pasture ecotone 1 0 1 0 0 Tec-5-97 Hay meadow 1 0 0 0 0 Tec-6-97 Woodland-pasture ecotone 1 1 1 0 0 Ull-4-96 Hay meadow also used for grazing 1 1 0 0 0 Ull-5-96 Hay meadow also used for grazing 1 1 1 1 0 Ull-6-96 Hay meadow also used for grazing 1 1 0 0 0 Ull-7-96 Hay meadow also used for grazing 1 1 0 0 0 (continued on next page) 244 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246

Appendix A (continued) Section label Habitat description Categorical habitat variables Grassland Cattle Woodland Bramble Arable cover grazing cover cover Weld Vil-1-89 Dry pasture 1 1 0 0 0 Vil-2-89 Hay meadow also used for grazing 1 1 0 0 0 Vil-4-89 Hay meadow also used for grazing 1 1 0 0 0 Vil-5-89 Hay meadow also used for grazing 1 1 0 0 0 Vil-7-89 Dry pasture 1 0 0 1 0 Vil-8-89 Hay meadow 1 0 0 0 0 Vil-10-89 Woodland ride 0 0 2 1 0 Vil-11-89 Woodland ride 0 0 2 1 0 Relative grassland cover (0: <30%; 1: >30%); cattle grazing (0: absence; 1: presence); relative woodland cover (0: absence; 1: 10–30%; 2: >30%); rela- tive bramble cover (0: absence; 1: 10–30%; 2: >30%); arable Welds at the sides of the recording route (0: absence; 1: presence).

Appendix B

Summary of the life-history attributes for the 47 butterXy species considered in this study Body size Overwintering Voltinism Host-plant Dispersal Rarity1 Rarity2 (wing length stage specialization ability (regional (local scale) in mm) scale) Carcharodus alceae 14.5 2 3 2 2 0.02 0.04 Carcharodus boeticus 13.5 2 3 2 0 0.11 1.00 Ochlodes venata 15.5 2 2 2 1 0.03 0.02 Pyrgus armoricanus 13 2 2 1 1 0.05 0.11 Pyrgus malvoides 12 3 2 2 1 0.03 0.08 Spialia sertorius 12 2 2 1 0 0.03 0.33 Thymelicus acteon 12 2 1 2 1 0.02 0.08 Aricia cramera 12 2 3 2 1 0.02 0.06 alcetas 14.5 2 3 1 2 0.10 1.00 Celastrina argiolus 15 3 3 3 3 0.02 0.05 Cacyreus marshalli 11.5 5 3 2 2 0.05 1.00 Cupido argiades 12.5 2 3 2 2 0.11 0.25 Lampides boeticus 16.5 5 3 3 4 0.02 0.06 Lycaena phlaeas 13.5 2 3 2 2 0.02 0.04 Leptotes pirithous 12.5 5 3 3 4 0.02 0.04 Plebejus argus 13.5 2 3 3 0 0.07 0.05 Polyommatus icarus 16 2 3 2 2 0.02 0.02 Satyrium w-album 15.5 1 1 1 0 0.25 1.00 Cynthia cardui 28 5 3 3 4 0.02 0.03 Inachis io 28 4 3 1 3 0.05 0.08 Issoria lathonia 21 3 2 3 0.05 1.00 Melitaea cinxia 18 2 2 1 1 0.07 1.00 Melitaea didyma 21 2 2 2 2 0.04 0.14 Melitaea phoebe 22 2 2 2 2 0.03 0.50 Polygonia c-album 23 4 3 3 3 0.04 0.06 Vanessa atalanta 29.5 2 3 3 4 0.02 0.05 Papilio machaon 35 3 3 3 4 0.02 0.05 Anthocharis cardamines 21.5 3 1 2 2 0.04 1.00 Colias crocea 25 2 3 2 4 0.02 0.02 crameri 22 3 2 2 1 0.02 0.08 Gonepteryx cleopatra 27.5 4 2 1 3 0.02 0.20 C. Stefanescu et al. / Biological Conservation 126 (2005) 234–246 245

Appendix B (continued) Body size Overwintering Voltinism Host-plant Dispersal Rarity 1 Rarity 2 (wing length stage specialization ability (regional (local scale) in mm) scale) Gonepteryx rhamni 28 4 1 1 3 0.03 0.25 Leptidea sinapis 21.5 3 3 2 1 0.02 0.17 Pieris brassicae 30.5 3 3 2 4 0.02 0.02 Pontia daplidice 22.5 3 3 3 4 0.02 0.17 Pieris mannii 21.5 3 3 2 1 0.07 0.50 Pieris napi 25 3 3 2 3 0.03 0.02 Pieris rapae 25 3 3 2 4 0.02 0.02 Brintesia circe 34.5 2 1 2 1 0.03 0.17 Coenonympha pamphilus 15 2 3 2 1 0.04 0.03 Lasiommata megera 22 2 3 2 2 0.02 0.03 Maniola jurtina 25.5 2 1 2 2 0.02 0.04 Melanargia lachesis 26.5 2 1 2 1 0.03 0.03 Melanargia occitanica 26.5 2 1 1 0 0.06 0.50 Pararge aegeria 20.5 2.5 3 2 2 0.02 0.02 Pyronia cecilia 15.5 2 1 1 1 0.02 0.07 Pyronia tithonus 18 2 1 2 1 0.04 0.04 Overwintering stage: 1 – egg, 2 – larva; 3 – pupa; 4 – adult; 5 – no overwintering and/or migratory species (no category was assigned to Issoria lathonia, which overwinters as larva, pupa or adult; Pararge aegeria overwinters as larva or pupa). Voltinism: 1 – univoltine, 2 – bivoltine; 3 – multivoltine. Host-plant specialization: 1 – monophagous, 2 – oligophagous; 3 – polyphagous. Dispersal ability: 0 – forming closed populations, very little dispersal; 1 – closed populations, more frequent dispersal, 2 – closed populations, common dispersal, 3 – open populations, non-directional dispersal, 4 – open populations, directional migration. Rarity at regional scale is deWned as the inverse of the number of CBMS sites in which a species occurred (from a total of 54). Rarity at the local scale is deWned as the inverse of the number of sections in the AENP in which a species occurred (from a total of 46). Data from Higgins and Riley (1984), Pollard and Eversham (1995), Dennis and Shreeve (1996), Tolman and Lewington (1997) and personal observa- tions.

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