J Conserv DOI 10.1007/s10841-013-9567-7

ORIGINAL PAPER

Oviposition preferences of a threatened butterfly morsei (: ) at the western border of its range

Tatjana Cˇ elik

Received: 30 October 2012 / Accepted: 7 April 2013 Ó Springer Science+Business Media Dordrecht 2013

Abstract The oviposition preferences of Leptidea morsei Introduction at the western border of its range (SE Slovenia) were studied with the aim of integrating this information into Woodland butterflies require open and sunny habitats species habitat management recommendations. The char- within forests, such as sparse stands, clearings, rides, roads, acteristics of egg-laying habitat were examined at the trails and forest edges. Traditional woodland management landscape, patch, plant and leaf levels. Because sightings of practices (e.g. coppicing, pollarding, pannage, burning) adults in the field were infrequent, intensive searching for maintained an open and highly diversified structure of previously laid eggs on plants was chosen European woodlands for millennia (Settele et al. 2009). as the survey method. The main oviposition habitats of During the last decades, modern forestry has changed many L. morsei in Slovenia were found to be the forest edges and of those woodlands resulting in dense and structurally light stands of thermophilous oak, oak-hornbeam and uniform stands. The loss of open woodlands has led to a mesic beech forests (landscape level). The egg-laying sites rapid decline in the woodland butterfly species distribution were L. niger plants growing individually or in small (-14 %) across Europe over the last 25 years (van Sway stands, and oriented mostly towards W, SW, and S. The et al. 2006). oviposition plants were between 33 and 120 cm high, with Among twenty-nine butterfly species listed on the those growing in half to full shade preferred. Eggs were Annexes of the Habitats Directive (cf. Van Sway et al. deposited singly, mainly on the underside of leaflets of 2012), twelve are considered woodland species (Settele terminal leaves, located mostly on the top quarter of plants et al. 2009), including Leptidea morsei (Fenton 1881), a irrespective of their height and growth form. The most species classified as Near Threatened in Europe and as important factors affecting egg-placement are sun exposure Endangered in the EU-27 (Van Swaay et al. 2010). It has and the size of L. niger stands at ovipositing sites (patch been known for more than a decade that L. morsei has level), leaf exposure on the plant in vertical and horizontal declined in distribution in Europe by 50–80 % (Van Sway directions (plant level), leaf age and the leaf parts where and Warren 1999). Today, the species’ European distri- the risk of leaf and egg desiccation is lower (leaf level). bution range occupies only 3.55 % of the area of Europe Management strategies for the main egg-laying habitats of (Kudrna et al. 2011). The Climatic Risk Atlas of European the species are proposed. Butterflies (Settele et al. 2008) placed the species in a category of ‘‘very high climate change risk (HHR)’’ due to Keywords Leptidea morsei Lathyrus niger Butterfly the 85 % loss of its current grid cells under at least one of conservation Oviposition preference Forest management the three simulated scenarios. Despite L. morsei’s high threatened status and unfa- vourable predictions for long term survival at the western T. Cˇ elik (&) part of its distribution range, very little information is Jovan Hadzˇi Institute of Biology, Scientific Research Centre available on its life history, ecology and appropriate habitat of the Slovenian Academy of Sciences and Arts, Novi trg 2, P. O. Box 306, 1001 Ljubljana, Slovenia management. In Europe, the main habitats of the species e-mail: [email protected] are sparse deciduous and mixed woods predominantly with 123 J Insect Conserv oaks (Quercus petraea Liebl., Q. cerris L.), European Therefore, this study defines the main characteristics of Hornbeam (Carpinus betulus L.) and Sweet Chestnut L. morsei oviposition habitat at the western border of the (Castanea sativa Mill.), edges of woods, forest islands, species range (SE Slovenia) and integrates this information roads and clearings, and shrubland on abandoned grass- into habitat management recommendations. As egg-laying lands (Lorkovic´ 1927, 1950, 1975, 1993;Ho¨ttinger 2004; involves processes that occur at different spatial scales Cˇ elik et al. 2005; Gascoigne-Pees et al. 2008). To date, the in a hierarchical fashion, e.g. selection of parts within only confirmed ovipositing and host plants of the species in plant, plants within host plant patches, patches within Europe are Lathyrus niger Bernh. (Lorkovic´ 1950, 1975; landscape (Rabasa et al. 2005), the oviposition preferences Ho¨ttinger 2004; Gascoigne-Pees et al. 2008) and the of L. morsei was examined on landscape, patch, plant and endemic L. hallersteinii Baumg. in Transylvania (Van leaf level, and the relative importance of factors from each Sway et al. 2012). Preliminary observations on previously level for oviposition site selection was evaluated. deposited eggs on L. niger plants in Slovenia and Romania (Gascoigne-Pees et al. 2008) showed that eggs are laid singly on the underside of leaves of plants in shaded forest Methods growth. L. morsei is an Euro-Siberian species, distributed from Study sites Eastern Europe across temperate Siberia, Mongolia, the northern China and Korea to northern Japan (Kudrna et al. At its westernmost range limit, in Slovenia, L. morsei is 2011). Habitat occupancy varies across the Palaearctic distributed in the south-eastern part of the country (Fig. 1). region, ranging from forest complexes in the western to Three sites in Slovenia were included in this study: (1) open meadows at the eastern part of its distribution western edge of Bela krajina region (45°360N, 15°80E), (2) (Lorkovic´ 1993). For the successful conservation of any Kolpa River valley (45°290N, 15°20E) and (3) southern edge species, knowledge of its habitat preferences at local scales of Posavsko hribovje region (46°00N, 14°590E) (Fig. 1). In across a species’ range is required (e.g. Anthes et al. 2008), Bela krajina region, the main area of L. morsei distribution in and an understanding of the perceptual world of the target Slovenia, the species is mainly continuously distributed. organism and its interactions with the environment is The other two sites are considered as isolated populations desired. In rapidly changing anthropogenic landscapes, an (Verovnik et al. 2011). Common characteristics of all three adoption of the functional habitat model based on species- sites are mesic and thermophilous deciduous and mixed specific resource distribution and individual movements forests on calcareous bedrock with more than 1100 mm (Dennis 2003; Dennis et al. 2006) is one of the most of rainfall annually (Marincˇek and Cˇ arni 2002; Marincˇek appropriate ways to translate human observed structural et al. 2006). habitats into organism-centred functional space (Van Dyck Study site 1 (area c. 45 km2, altitude 200–750 m) consists 2012). The resource-based habitat concept considers all life of an extensive forest complex with forest roads, small stages of an organism and thus offers an advanced oppor- clearings and grasslands on a plateau, which on its eastern tunity for successful conservation management of threa- side drops to extensively used agricultural landscape with tened butterfly species. From this point of view, the forest islands, hedges and scrub on abandoned grasslands. understanding of a species’ oviposition site preferences This site is dominated by thermophilous Illyrian oak-horn- may be of crucial importance because an oviposition itself beam forests (Abio albae-Carpinetum betuli Marincˇek 1994) represents the spatial interface between all four successive with Quercus petraea Liebl., Carpinus betulus L., Acer life stages (adult, egg, larvae, pupa) and the environment campestre L. and Picea abies Karsten (Marincˇek and Cˇ arni (Garcia-Barros and Fartmann 2009). Considering that (1) 2002). These forests cover the larger part of the plateau the knowledge of the ecology of L. morsei is still poor and (altitude: 400–600 m) and grow also in forest islands in the comparable data from Europe are lacking (Van Sway et al. agricultural lowland. Mesic beech forest (Lamio orvale- 2012), (2) the information on appropriate management Fagetum Borhidi 1963), dominated by Fagus sylvatica L. required to prevent species’ further decline is still insuffi- and Acer pseudoplatanus L., covers the westernmost part of cient, and (3) geographical variation of oviposition site plateau at altitudes above 600 m (Marincˇek and Cˇ arni 2002). preferences is already known in butterflies (e.g. Chew and The oak-hornbeam forests are managed predominantly by Robbins 1989; Freese and Fiedler 2002; Benesˇ et al. 2003; small-area group selection systems, and by coppicing in the Friberg et al. 2008a, b; Garcia-Barros and Fartmann 2009), agricultural lowland. Small-area group selection system and information on oviposition habitat of L. morsei at its irregular shelterwood system are the prevailing practices in western range limit is important for the understanding of its high beech forest (Zavod za gozdove Slovenije 2006, 2011a). ecological requirements, particularly from the functional Study site 2 (area 20 ha, altitude 200–300 m) is a habitat viewpoint. light thermophilous oak-hornbeam forest (Abio albae- 123 J Insect Conserv

Fig. 1 Current distribution of Leptidea morsei in Slovenia (modified from Verovnik et al. 2012) and the location of three study sites: 1—western edge of Bela krajina region, 2—Kolpa River valley, 3—southern edge of Posavsko hribovje region

Carpinetum betuli Marincˇek 1994) dominated by Q. pet- adults (cf. Gascoigne-Pees et al. 2008). Thus, following raea, C. betulus and A. campestre. It is located on a individual egg-laying females and observations of their southern slope above the river Kolpa and managed as a egg-laying are not appropriate field methods for this spe- forest with important protection functions (Zavod za goz- cies. During my study only two females were observed dove Slovenije 2011b). These include the protection egg-laying, each of them only laying one egg. Therefore against soil erosion from wind and water. eggs were located by searching for previously laid eggs, Study site 3 (area 70 ha; altitude 440–650 m) is a hilly exclusively on L. niger plants. To avoid a bias towards any area with a mosaic of extensively used agricultural land expected habitat characteristics, I used an intensive (predominantly vineyards and orchards) and thermophilous searching method. Hence, at study site 2, the whole area oak and mesic beech forests on ridges and mainly sunny was searched for L. niger plants, which were investigated slopes. In light oak forests (Lathyro nigrae-Quercetum for eggs. In study sites 1 and 3, the areas not suitable for petraeae Horvat 1958) the tree layer consists of Q. petraea, L. morsei (i.e. cultivated areas, dense forests) were exclu- O. carpinifolia, Sorbus aria Crantz., F. ornus, Quercus ded from the survey, and searching for L. niger plants was cerris L. and A. campestre. They are managed as forests spatially regular. At sampling locations where L. niger was with important protection functions (Marincˇek et al. 2006). abundant, examined plants were chosen randomly. Dominating tree species in the beech forests (Hacquetio The characteristics of L. morsei oviposition habitat were epipactis-Fagetum Kosˇir 1962) are F. sylvatica, Q. pet- recorded at landscape, patch, plant and leaf levels. For each raea, C. betulus and A. campestre (Marincˇek et al. 2006). found egg I determined the following parameters: (1) Prevailing forest management practices are small-area landscape level: HT—habitat type (light forest stand; forest group selection systems and irregular shelterwood systems edge—including rides, forest roads, trails and outer edges (Zavod za gozdove Slovenije 2011c). of forests; regenerating woodland on grassland); (2) patch level: LnS—amount of L. niger plants at the oviposition Study of oviposition habitat site, i.e. an area of 5 9 5 m with the oviposition plant in the centre of the plot (individually/small stand: B5 plants; The study was undertaken during the peak of the first medium-sized stand: 6–50 plants; large stand:[50 plants), generation of L. morsei in 2011 (5–18 May). The popula- As—aspect of an oviposition site (N, E, S, W, NE, NW, tion density of L. morsei at all three study sites is low SE, SW), SE—sun exposure of an oviposition site (1—full (Verovnik et al. 2011) resulting in infrequent sightings of sun, 2—half shade, 3—full shade); (3) plant level:

123 J Insect Conserv

PH—plant height, GF—growth form of the plant (number assessing within- and inter-level prediction power of of lateral shoots: 0—no lateral shoots, 1—one or two lat- parameters respecting their hierarchical order (land- eral shoots, 2—three or four lateral shoots, 3—five or more scape [ patch [ plant [ leaf). The prediction power of lateral shoots), OH—oviposition height, ENo—number of parameters was determined by the value of asymmetric eggs per plant (1 egg/plant; [1 egg/plant); (4) leaf level: Goodman and Kruskal’s Lambda statistic and its signifi- lP—part of egg-bearing leaf (adaxial/abaxial surface of the cance. Since the value reflects the percentage reduction in leaflet; rachis), lT—type of egg-bearing leaf (I—leaf on the error in predicting the dependent variable given the known stem, II—leaf on the lateral shoot), lA—relative age/posi- independent variable, the comparison between Lambda tion of egg-bearing leaf (determined by counting leaves values was performed only among independent variables from the tip of stem/lateral shoot downwards). For each of testing for the same dependent variable. In each compari- the unoccupied plants I recorded the same landscape and son, the parameter assigned as dependent variable derived patch parameters as for the occupied ones. from the same or lower hierarchical level than parameters which were used as independent variables. All parameters, Statistical analyses except ‘‘habitat type (HT)’’ which is a single parameter at the highest hierarchical level, were tested as dependent Data from 5 oviposition plants were incomplete, and were variables. therefore excluded from analyses of plant and oviposition All statistical analyses were performed using SPSS 13.0 height, leaving 37 plants and 46 eggs (total: 42 plants, 52 (SPSS Inc. 1989–2004). eggs). It is impossible to determine if eggs on a plant belong to one or more females, therefore each egg was treated as a single data point. Results To define the oviposition preferences at the landscape and patch levels, the comparison of absolute frequencies Egg distribution patterns between occupied and unoccupied plants was performed using Likelihood ratio statistic. Standardized residuals In total, I surveyed for L. morsei eggs on 167 L. niger were used to define the significant contributors to the plants (site 1: N = 136, site 2: N = 6, site 3: N = 25). On overall Chi square value. Oviposition preferences at the forty-two occupied plants (site 1: N = 36, site 2: N = 1, plant and leaf levels were evaluated by testing the egg site 3: N = 5) I found 52 eggs (site 1: 45; site 2: 2; site 3: distribution for homogeneity using Pearson Chi square test. 5; Table 1b, c, d), corresponding to an average egg loading To detect the relationships between landscape, patch, of 33 %, 33 % and 20 % for sites 1, 2 and 3, respectively. plant and leaf parameters of the occupied plants, Chi All eggs were deposited singly. All plants found at site 2 square tests using Likelihood ratio statistic were applied grew individually in full shade, within light forest, and because of small sample sizes which resulted in expected occurred in S or SW aspects (Table 1c). At site 3, most of frequencies lower than 1 in some cases. For assessing the the aspects and all categories of habitats, sun exposure and strength of association between parameters, Cramer’s L. niger stands were available for oviposition (Table 1d). V was used. For the purpose of Chi square testing, the Due to low sample sizes, data from the sites 2 and 3 values of interval parameters (i.e. PH, OH) were arranged were merged and then tested against data from site 1 for the in the following frequency classes: 0–20 cm, 21–40 cm, differences between occupied/unoccupied plants on land- 41–60 cm, 61–80 cm, 81–100 cm and 101–120 cm. Forest scape and patch levels. I found significant differences edge and regenerating woodland on grassland were com- between sites (site 1 vs. sites 2 and 3) for each landscape bined (i.e. non-forest) for testing the relationship between and patch parameter of the unoccupied plants, whereas the habitat type and other parameters. The Jonckheere–Terp- occupied plants of site 1 differed from those of sites 2 and 3 stra test was used to test for an ordered pattern of medians only in aspect (Table 1e). Hence, data from all sites were for both interval parameters (PH, OH) across the categories merged for evaluation of oviposition preferences at land- of two nominal parameters, ‘‘sun exposure of an oviposi- scape and patch levels. The occupied and the unoccupied tion site’’ (SE) and ‘‘growth form of egg-bearing plant’’ plants differed significantly in all measured landscape and (GF). By applying this test the directions of relationships patch parameters (Table 1a): eggs were predominantly laid between interval and nominal parameters were evaluated. on plants growing individually/in small stands (50 %) in A non-parametric Kendall’s tau correlation coefficient was half or full shade (92 %) at the forest edge (67 %) or in applied for additional estimation of the strength of the light forest stands (27 %), whereas plants exposed to full relationship between both interval parameters. sun (stand. residual =-3.2) or those growing in large L. The relative importance of landscape, patch, plant and niger stands (stand. residual =-2.0) or on abandoned leaf characteristics for egg-placement was evaluated by grasslands (stand. residual =-2.6) were avoided. Females 123 netConserv Insect J

Table 1 Absolute (N) and relative (%) frequencies of the landscape and patch parameters at unoccupied and occupied plants (Lathyrus niger)ofLeptidea morsei in SE Slovenia in 2011. Likelihood ratio statistics (LR) are presented for comparisons of absolute frequencies between unoccupied and occupied plants (a–d), and between unoccupied/occupied plants of site 1 and sites 2 and 3 (e) Parameter (a) (b) (c) (d) (e) All sites Site 1 Site 2 Site 3 Site 1 vs. Sites 2 and 3 Unoccupied Occupied Unoccupied Occupied Unoccupied Occupied Unoccupied Occupied Unoccupied Occupied (N = 125) (N = 52) (N = 100) (N = 45) (N = 5) (N = 2) (N = 20) (N = 5) N%N%N%N%N%N%N%N%

Habitat type LR = 15.20, df = 2, p \ 0.01 LR = 18.95, df = 2, p \ 0.001 # LR = 5.15, df = 2, p = 0.076 p \ 0.001 p = 0.639 Light forest stand 19 15 14 27 8 8 12 27 5 100 2 100 6 30 0 0 Forest edge 69 55 35 67 58 58 30 67 0 0 0 0 11 55 5 100 Abandoned grassland 37 30 3 6 34 34 3 6 0 0 0 0 3 15 0 0 Aspect LR = 34.24, df = 7, p \ 0.001 LR = 41.35, df = 7, p \ 0.001 # LR = 9.86, df = 4, p \ 0.05 p \ 0.05 p \ 0.01 N 119009900000021000 NE 7612771200000000 E 171436 171737 00000 0 00 SE 28 22 6 12 20 20 6 13 0 0 0 0 8 40 0 0 S 41331529323281836021006305100 SW 14 11 11 21 10 10 11 24 2 40 0 0 2 10 0 0 W 321223111227000021000 NW 4348444900000000 Sun exposure LR = 26.56, df = 2, p \ 0.001 LR = 30.09, df = 2, p \ 0.001 # LR = 4.86, df = 2, p = 0.088 p \ 0.05 p = 0.551 Full sun 56 45 4 8 50 50 3 7 0 0 0 0 6 30 1 20 Half shade 34 29 24 46 27 27 20 44 0 0 0 0 7 35 4 80 Full shade 35 26 24 46 23 23 22 49 5 100 2 100 7 35 0 0 Size of L. niger stand LR = 9.95, df = 2, p \ 0.01 LR = 8.10, df = 2, p \ 0.05 # LR = 7.17, df = 2, p \ 0.05 p \ 0.05 p = 0.335 Ind./small (B 5 plants) 39 31 26 50 27 27 22 49 5 100 2 100 7 35 2 40 Medium (6-50 plants) 43 34 19 37 40 40 16 36 0 0 0 0 3 15 3 60 Large ([ 50 plants) 43 34 7 13 33 33 7 16 0 0 0 0 10 50 0 0 # Sample sizes are too low for comparison 123 J Insect Conserv

Fig. 3 The distribution of plant and oviposition height of Leptidea morsei in SE Slovenia in 2011

Fig. 2 Polarplot of the aspects (in %) of unoccupied L. niger plants (grey line,N= 125) and egg-laying sites (black line,N= 52 eggs) of first generation of Leptidea morsei in SE Slovenia in 2011

Table 2 Results of Chi square tests for homogeneity for analyzing the egg distribution of Leptidea morsei at plant and leaf levels Parameter Pearson Chi df p value square

Plant height 28.4*** 5 0.000 Oviposition height 59.7*** 5 0.000 Plant growth form 2.3 3 0.511 No. of eggs per plant 13.4*** 1 0.000 Leaf part 27.8*** 1 0.000 Leaf type (all plants) 13.0*** 1 0.000 Fig. 4 Oviposition height of Leptidea morsei in percentage of the Leaf type (plants with lateral 3.3 1 0.071 plant height (Lathyrus niger) in SE Slovenia in 2011. Black line shoots) represents median, broken lines represent 1st and 3rd quartiles Leaf age 14.2* 5 0.014 At plant and leaf levels, the egg distribution significantly * p \ 0.05, *** p \ 0.001 departed from homogeneity for all parameters, except for the growth form of egg-bearing plants and the leaf type of preferentially oviposited in sites oriented towards the west plants with lateral shoots (Table 2). (23 %) and south-west (21 %), while they completely There was a significantly higher number of eggs (67 %) avoided the northern orientation (Fig. 2). Sites 2 and 3 than expected found on plants that were 41–80 cm high significantly differed from site 1 in the aspects used for (Fig. 3). Half of the egg-bearing plants were of between 50 oviposition (Table 1e): higher number of eggs than and 73 cm high (min: 33 cm, max: 120 cm; Fig. 4). The expected were laid on plants exposed to the south at sites 2 vertical position of the eggs ranged from 23 to 102 cm, but and 3. Yet, the preference for the plants oriented toward the the majority (57 %) was located 41–60 cm above the south may simply be biased due to small sample size (sites ground (Fig. 3). All eggs were deposited above 62 % of the 2 and 3 = 7 eggs), since the lower acceptance of southern plant height (median: 85 %, 1st and 3rd quartiles: 78 % exposition than expected at site 1 (Table 1b) was not sig- and 90 %, max: 100 %; Fig. 4), and 83 % of eggs were nificant (stand. residual =-1.3). At site 1, there is also a located on the top quarter of the plants. There was no possibility that occupied plants exposed to the south may correlation between oviposition height as percentage of the be underrepresented because of the overall unfavourable plant height and height of egg-bearing plants (Kendall characteristics of L. niger plants available in this aspect: s =-0.032, p [ 0.7). 84 % of unoccupied plants were exposed to full sun, but The distribution of eggs according to the number of those growing in half or full shade were located either in lateral shoots on oviposition plants showed no preference large stands (9 %) or on abandoned grasslands (3 %). for particular plant growth form. One egg per plant was 123 J Insect Conserv

irrespective of leaf type (Fig. 6), which corresponds with the terminal and young parts of the plant.

The importance of landscape, patch, plant and leaf characteristics for egg-placement

Between landscape and patch level, there were two sig- nificant relationships between parameters, with the stron- gest association between the habitat type and sun exposure (Table 3). The number of eggs deposited in light forests was positively associated with full shade (100 %) and with the plants growing individually or in small stands (86 %); in non-forest habitats 26 % and 37 % of eggs were laid in Fig. 5 The distribution of Leptidea morsei eggs depending on plant full shade (63 % in half shade, 11 % in full sun) and on growth form and sun exposure of an oviposition site in SE Slovenia in plants in small stands (50 % in medium, 13 % in large), 2011 respectively. At the patch level, there were two significant relation- ships between parameters (Table 3). The western oriented egg-laying sites were positively related to the eggs laid in full shade (83 %) and to the egg-bearing plants growing individually (83 %). The percent of eggs laid in full shade increased from SE to W orientation (SE–S–SW–W: 17, 20, 55, 83 %) and decreased for eggs laid in half shade (83, 60, 45, 17 %). The same pattern was observed for amount of L. niger plants at the oviposition site: the percent of eggs deposited in small stand increased from SE to W orienta- tion (33, 40, 18, 83 %) and decreased for eggs laid in medium stand (67, 40, 55, 17 %). The distribution of eggs regarding the sun exposure of the oviposition site was better predicted by habitat type (k = 0.500, p = 0.011) than by orientation of oviposition site (k = 0.357, p = 0.013). The sun exposure was a better predictor of egg distribution regarding the orientation (k = 0.189, p = 0.044) than the size of L. niger stands (k = 0.108, Fig. 6 Percentage of Leptidea morsei eggs depending on type p = 0.313). The latter was better predicted by orientation (Roman numerals) and relative age (Arabic numerals) of egg-bearing of oviposition site (k = 0.269, p = 0.062) than by habitat leaf. I—leaf on the stem, II—leaf on the lateral shoot, 1—the type (k = 0.192, p = 0.381). youngest (uppermost) leaf, 6—the oldest (the lowest) leaf At the plant level, there were three significant relation- ships between parameters, with the strongest relationship found in 79 % of cases (33 plants); in eight plants I found between the plant and oviposition height (Table 3). Ovi- two eggs, these were found on the same leaf in three cases. position height correlated positively with plant height In one plant I found three eggs, all being on the same leaf. (Kendall’s s = 0.747, p \ 0.001). It also increased with In all four cases with more than one egg per leaf, eggs were the number of lateral shoots on the plant (Jonckheere– placed on different leaflets. The majority of eggs (86 %) Terpstra z = 3.87, No. of levels = 4, p \ 0.001) as the were placed on the abaxial surface of the leaflets, six eggs result of the positive relationship between plant height and (12 %) on adaxial surface of the leaflet, and one egg on the its growth form (Jonckheere–Terpstra z = 5.13, No. of rachis (i.e. the main stem of the compound leaf). Thirty- levels = 4, p \ 0.001). seven eggs (71 %) deposited on plants with lateral shoots At landscape–plant and patch–plant levels, there were (Fig. 5) were homogeneously distributed between both leaf eight significant relationships between parameters (Table 3). types. Egg placement differed with leaf age, with a higher Major contributors to significant relationships of the height number of eggs than expected on second and third leaves, of egg-bearing plants were positive associations between (1) and lower number of eggs than expected on the sixth leaf. plants of 21–40 cm high and light forest (36 %), (2) plants of Hence, 88 % of eggs were located on the first four leaves 101–120 cm high and full sun (33 %), and (3) plants of 123 J Insect Conserv

Table 3 Results of testing the relationships between parameters used for description of the oviposition habitat of Leptidea morsei in SE Slovenia in 2011 at four hierarchical levels: landscape (HT), patch (As, SE, LnS), plant (PH, GF, OH, ENo) and leaf (lP, lT, lA) HT As SE LnS PH GF OH ENo lP lT lA

HT 0.472 0.656*** 0.478** 0.584** 0.311 0.502* 0.434** 0.015 0.150 0.415 As 0.070 0.452* 0.457* 0.421 0.501** 0.449 0.536 0.362 0.533* 0.359 SE 0.000 0.029 0.141 0.448* 0.459** 0.507** 0.296 0.210 0.092 0.469* LnS 0.001 0.011 0.816 0.403 0.136 0.352 0.352 0.195 0.142 0.374 PH 0.003 0.145 0.028 0.028 0.565*** 0.660*** 0.377 0.126 0.192 0.294 GF 0.197 0.000 0.003 0.950 0.000 0.421** 0.317 0.165 0.254 0.406* OH 0.017 0.070 0.017 0.400 0.000 0.006 0.265 0.165 0.117 0.290 ENo 0.013 0.093 0.158 0.085 0.340 0.322 0.637 0.389* 0.217 0.256 lP 1.000 0.196 0.381 0.331 0.954 0.713 0.898 0.028b 0.098 0.410 lT 0.472 0.010 0.886 0.615 0.892 0.340a 1.000 0.209c 0.664 0.356 lA 0.111 0.263 0.003 0.151 0.694 0.065 0.899 0.674 0.124 0.242 The Cramer’s V are shown in the top right hand part and p values of Likelihood ratio statistic at the bottom of the table. See methods for an explanation of the parameters and the statistical tests used The significant relationships between parameters are presented in bold * p \ 0.05, ** p \ 0.01, *** p \ 0.001 a Only plants with lateral shoots were included in Chi square test because the expected frequency in the cell ‘‘branchless plants/leaf type II’’ could not be different from zero b Plants with 2 or 3 eggs which were placed in combination abaxial/adaxial surface of leaflets were added into category ‘‘adaxial’’ because in this combination the expected frequency for plants with one egg could not be different from zero. In Chi square test this means that in the cell ‘‘adaxial/plants with more than 1 egg’’, plants with both combinations (i.e. adaxial/adaxial, abaxial/adaxial) were included c Plants with 2 or 3 eggs which were placed in combination leaf type I/II were added into category ‘‘leaf type II’’ because in this combination the expected frequency for plants with one egg could not be different from zero. In Chi square test this means that in the cell ‘‘leaf type II/plants with more than 1 egg,’’ plants with both combinations (i.e. II/II, I/II) were included

41–60 cm high and medium stand of L. niger plants (56 %). p = 0.009; OH: k = 0.450, p = 0.003) than by landscape The parameter which best predicted the height of egg- or patch parameters (As and SE as predictors for GF: bearing plants was sun exposure (k = 0.233, p = 0.080; HT k = 0.333, p = 0.002 and k = 0.250, p = 0.041; HT and as predictor: k = 0.133, p = 0.092, LnS as predictor: SE as predictors for OH: k = 0.000, p = 1 and k = 0.050, k = 0.133, p = 0.341) and plant height increased with the p = 0.312). The number of eggs per plant was only related sun exposure (Jonckheere–Terpstra z = 3.13, No. of lev- with habitat type in respect to inter-level associations els = 3, p \ 0.01). Considering the growth form of egg- (Table 3). There was a significant positive association bearing plants, there were significantly more eggs than between plants with more than one egg and light forest expected laid on (1) branchless plants in western oriented (56 %); in non-forest habitats only 12 % of plants had egg-laying sites (58 %), (2) plants with 1 or 2 lateral shoots more than one egg. Plants with more than 1 egg appeared in SW orientation (46 %), (3) plants with 3 or 4 lateral in small (8 cases) and large L. niger stands (1 case), but the shoots in SE orientation (67 %), and (4) luxuriant plants in relationship between both parameters (ENo, LnS) was only NW orientation of egg-laying site (50 %). No eggs were marginally significant (Table 3). deposited on branchless plants in S orientation (i.e. sig- Within leaf level, there were no significant relationships, nificant negative association: stand. residual =-2.1). but leaf parameters were related with plant (GF, ENo) and Significant positive associations were found between (1) patch (As, SE) parameters (Table 3). The only contributor eggs deposited in full shade and branchless egg-bearing to a relationship between leaf part and egg number per plants (50 %), (2) eggs in half shade and plants with 1 or 2 plant was a higher number of plants than expected with 2 or lateral shoots (38 %), and (3) eggs in full sun and luxuriant 3 eggs placed in the following combinations: all eggs on plants (75 %) (Fig. 5). Considering the oviposition height, upper side of the leaves, or some eggs on upper side and there were significant positive associations between (1) some on the underside of leaves; 44 % of plants with more plants of 21–40 and 61–80 cm high (38 % and 29 %) and than one egg had such combinations, and only 9 % of light forest, and (2) plants of 81–100 and 101–120 cm high plants with one egg had an egg on the upper side of leaf. (both 33 %) and ovipositing sites in full sun. Both, the The eggs laid on the leaves of lateral shoots were positively growth form of egg-bearing plants and oviposition height associated with southern orientation of egg-laying site were better predicted by plant height (GF: k = 0.387, (61 %), and negatively associated with SW (0 %) and W

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(8 %) oriented sites, but site orientation was not an oviposition period (April, May) in E Austria than in important predictor of egg distribution regarding the leaf SE Slovenia (http://www.worldweatheronline.com). This type (k = 0.077, p = 0.796). Egg distribution according to might be explained by the fact that butterflies require a leaf age was related to sun exposure of egg-laying site and compromise between sufficient humidity to avoid egg and plant growth form (Table 3). There were significant posi- host plant desiccation for optimal embryonic develop- tive associations between (1) the oldest (sixth) leaf and half ment and elevated solar radiation to speed up larval shade/plants with 3 or 4 lateral shoots, (2) the fourth leaf development (Anthes et al. 2008). Hence, females of and full sun/luxuriant plants, (3) the third leaf and half Austrian populations might have benefited by spreading shade/plants with 1 or 2 lateral shoots, and (4) the second their eggs in more shady conditions where the risk of plant leaf and full shade/plants with 3 or 4 lateral shoots. Sun withering is lower. exposure was more significant predictor of egg distribution The present study has shown that L. morsei ovipositing according to leaf age (k = 0.237, p = 0.014) than plant females select plants growing in shady conditions where growth form (k = 0.237, p = 0.052) due to only margin- the canopy of adjacent higher bushes or trees enables only ally significant relationship between the growth form and transitory direct sunlight at egg-laying sites. As ovipositing leaf age (p = 0.065, Table 3). sites orientations towards the W, SW and S were preferred, it is possible that (1) females compensate for the shady conditions of site orientations by selecting area where transitory direct radiation levels are high (and thus the site Discussion is relatively warm), or (2) the preferred orientations reflected the time of day when females are most active, i.e. This study showed that the main egg-laying locations of in the afternoon. Elevated ambient temperature appears to L. morsei in Slovenia, the species’ westernmost range, are be particularly important to woodland butterfly species forest edges and light stands of thermophilous oak, oak- because it may (1) increase the larval development rate and hornbeam and mesic beech forests. The egg-laying sites are decrease the larval mortality (McKay 1991), and (2) L. niger plants, growing individually or in small stands, and improve the female fecundity by increasing the time oriented mostly towards the south, south-west and west. available for egg-laying, and consequently increase the The plants used for the oviposition are between 33 and egg-laying rate (Davies et al. 2006). My study, though with 120 cm high and the majority of them grow in half to full a low sample size, revealed significant female avoidance of shade. The eggs are deposited singly on terminal leaves on L. niger plants growing in full sun. Egg depositions on such the top quarter of the plant. plants were rare and likely resulted from low female These results derive from the study of the first generation selectivity at the moment of host evaluation. This may be in L. morsei and female host plant preferences might vary either due to (1) its large egg load (i.e. body size) (e.g. between spring and summer generations. This was observed L. sinapis, Berger et al. 2012), (2) timing close to the dusk in the related species, Leptidea sinapis (Linnaeus, 1758), and (i.e. when less time remained for oviposition activity) (e.g. L. reali (Reissinger, 1989) (Friberg and Wiklund 2009). L. sinapis, Berger et al. 2012), or (3) male presence during Importantly, future studies on L. morsei should resolve if the oviposition (e.g. Pararge aegeria, Gibbs et al. 2005). species is in fact monophagous or oligophagous (L. niger, The importance of warm microclimatic conditions at L. hallersteinii) within the European range. The conclusions oviposition sites may also be the reason for female pref- reached here on oviposition preferences can only refer to erence for plants growing individually or in small stands patches occupied with L. niger plants. considering that in loosely-structured vegetation the sur- rounding of oviposition plant receives more sunlight than Oviposition preferences plants in condensed stands. Furthermore, suitable solitary plants are more discernible and accessible for egg-laying The preference of egg-laying females for forest edges females, which may reduce their searching time (i.e. pre- observed in this study is consistent with data from alighting decision of female, Janz 2002). Females of the Gascoigne-Pees et al. (2008), who reported on deposited related L. sinapis were found to inspect a higher number of eggs in the lower altitudes in this region of Slovenia. This non-hosts than hosts in pre-alighting phase, and could not contrasts with egg-laying observations of the first genera- make long-distance choices (Wiklund 1977; Friberg et al. tion from eastern Austria (Ho¨ttinger 2004), which found 2008b; Berger et al. 2012). Hence, assuming that solitary that females selected internal parts of forest more fre- L. niger plants contribute to lower searching time of quently than forest edges on rides and paths. Such prefer- L. morsei females without knowing their behaviour ence for more shady areas could be the consequence of involved in host finding and the types of cues involved in lower average precipitation (by about 40 %) in the this process, might be too speculative. 123 J Insect Conserv

My results show that height and growth form of egg- In some cases I also observed that leaflets of young bearing plants are positively related to sun exposure of terminal leaves were inverted which could be the reason for oviposition site. Together with the wide range of plant infrequent ovipositions (12 %) on the upper side of leaflets, heights used for oviposition (33–120 cm) this indicates that and for a weak positive relationship between plants with such span-width of plant heights is most probably the result more than 1 egg and egg placement on the upper side of of the availability of plants with particular heights and leaflets. growth forms in particular sun conditions (i.e. lower plants were more available in the full shade than in the sun). As The relative importance of landscape, patch, plant plant growth form and type of leaf did not affect the dis- and leaf characteristics in selection of egg-laying site tribution of deposited eggs, it is likely that plant architec- ture has no important role in female selection of The significant relationships between landscape, patch, plant oviposition plant; this is simply determined by female and leaf parameters of L. morsei oviposition habitat showed preference for plants growing in shady conditions. The that selection of oviposition sites is determined by charac- latter indicates that other oviposition cues, such as plant teristics operating at different hierarchical levels. The quality and microclimatic conditions (Garcia-Barros and within- and inter-level prediction power of parameters con- Fartmann 2009), could be more important in assessing sidering their hierarchical order (landscape [ patch [ individual host plant suitability than physical cues, i.e. plant [ leaf) is reflected in their relative importance in the plant size or its phenologic stage. process of egg-laying site selection. The deposition of most eggs (83 %) on the top quarter of The habitat type (landscape level) as the best predictor the plant suggests that oviposition height above ground is for egg distribution regarding the sun exposure of ovipos- determined primarily by the height of the available L. niger iting site, and no relationship between the latter and plants. No relationship between oviposition height and leaf amount of L. niger plants at the oviposition site due to type or its relative age (Table 3), and placement of 88 % of female preference for small and medium foodplant stands eggs on the first four leaves irrespective of leaf type indi- in all sun conditions (% of eggs in those stands in full cate that females preferentially select terminal positions on shade, half shade and full sun: 87, 88 and 75) indicate that plants in both vertical and horizontal directions. One reason sun exposure and size of L. niger stand are the most for female preference for terminal leaves might be a rela- important characteristics for oviposition site selection at tively warmer position which speeds up egg and larval patch level. Sun exposure was also the best predictor for development. As larval growth efficiency in butterflies is egg distribution regarding the height of oviposition plant related to leaf water and nutrients (e.g. Fartmann and (plant level) and the leaf age (leaf level). As height and Timmermann 2006), the egg placement at the terminal growth form of egg-bearing plants were simply determined parts of the food plant could also enable the newly-hatched by sun conditions at oviposition site, it seems very likely caterpillar to easily access high quality leaves. This pre- that sun exposure is the most important factor in the diction is in accordance with a study in the family Pieridae, selection of the oviposition plant. At the plant level, ter- where water content of leaves is known to be an important minal plant parts (i.e. leaves) in both, vertical and hori- oviposition cue (Chew and Robbins 1989). Considering zontal direction, located on the top quarter of plant height that sun exposure of egg-laying site was a better predictor were preferred for egg-placement. At the leaf level, the egg of egg distribution regarding the leaf age than plant growth distribution was related to leaves with lower probability for form, the inter-level relationship of sun exposure with leaf withering in particular sun condition, and to leaf parts (i.e. age is more likely due to female selection of leaves with a underside of leaflets) where also eggs were protected from lower probability of withering in particular sun condition direct sunlight. This suggests that sun exposure is an (i.e. older leaves in full sun and half shade vs. younger important factor for egg-laying females also at leaf level. leaves in full shade) than to the simple availability of plant Therefore, it is most possible that in the process of egg- growth forms in particular sun condition (i.e. older growth laying site selection L. morsei behaves similarly to both forms in full sun and half shade vs. younger growth forms related species L. sinapis and L. reali (Friberg et al. 2008a, b) in full shade). Despite the preference of ovipositing with habitat choice proceeding the host plant choice. females for terminal parts of plants, only 17 % of eggs were laid on the first leaf (irrespective of leaf type: I-1 or Conservation management II-1) which is likely the consequence of the leaf develop- mental phase. Additionally, in all cases in my study the first L. morsei is one of the least studied butterfly species in leaf was not fully developed yet, which may also have Europe, thus we have very scarce knowledge about the prevented females from holding onto the leaf whilst laying. actual threats and appropriate management needed to

123 J Insect Conserv enable the species long term survival. Detailed information moderate thermophilous L. niger also inside the forest. (6) on woodland management practices, which are unfavour- If large open space inside the forest is required (e.g. able for the species, are known from Austria (Ho¨ttinger clearing for bee-keeping) then linear shapes with higher 2004) and Slovenia (Cˇ elik et al. 2005); in these countries, perimeter/area ratio are probably more appropriate than the favouring of dense commercial forests, afforestation non-linear ones as there is a higher probability for indi- with conifers, indiscriminate elimination of road edge vidually growing L. niger plants in shady conditions at the vegetation, the use of herbicides and intensive woodland edge of such areas than in their central part. Namely, it is grazing are recognised as most likely threats for the more likely that large and dense stands of L. niger, which species. are avoided for oviposition, appear at the central sunny part Here, I showed that warm and humid microclimate of open space. (7) Finally, harmful woodland management appearing in shady parts of light forest stands and forest practices mentioned above (cf. Ho¨ttinger 2004;Cˇ elik et al. edges located on southern to western slopes is crucial for 2005) should not be implemented, with the aim of pro- L. morsei egg-laying females. In such conditions L. niger viding appropriate habitat management preventing the plants grow individually or in small stands in the shelter of further decline of L. morsei in Europe. the canopy of adjacent higher bushes or trees and protected from prolonged direct sunlight. According to my results Acknowledgments I thank to M. Kuntner and S. Kralj-Fisˇer for large (i.e. dense) stands of L. niger are not appropriate for useful comments on an earlier version of the manuscript, I. Sajko for making the map (Fig. 1) and two anonymous referees for suggestions oviposition, which contradicts the conservation manage- that greatly improved the manuscript. This study was funded by the ment proposed by Van Sway et al. (2012). Habitat man- Slovenian Research Agency (P1-0236) and the Ministry of Environ- agement strategy for L. morsei based on my research ment and Spatial Planning of the Republic of Slovenia (2511-10- should incorporate the following practices. (1) Due to a 250021). long and narrow species habitat on forest roads, paths, rides and outer forest edges, the appropriate technique of mowing edge herb vegetation should be rotational block References mowing performed in the autumn (i.e. at the end of larval development). (2) To ensure intermittent insolation at the Anthes N, Fartmann T, Hermann G (2008) The Duke of Burgundy transition zone between herbaceous and shrub/tree zone, it butterfly and its dukedom: larval niche variation in Hamearis lucina across Central Europe. J Insect Conserv 12:3–14 is important to maintain structurally diverse tree and shrub Benesˇ J, Vrabec V, Herˇman P (2002) Be˘la´sek vy´chodnı´. In: Benesˇ J, vegetation. (3) In extensive forests managed as high forests Konvicˇka M (eds) Moty´li Cˇ eske´ republiky: Rozsˇ´ırˇenı´ a ochrana I (e. g. mesic beech forests, Illyrian oak-hornbeam forests on (Butterflies of the Czeck Republic: Distribution and conservation higher altitudes in SE Slovenia) the most important man- I). SOM, Praha, pp 182–184 Benesˇ J, Konvicˇka M, Vrabec V, Za´mecˇnı´k J (2003) Do the sibling agement action for L. morsei is preservation of dense net- species of small whites, Leptidea sinapis and L. reali (Lepidop- work of forest roads and paths as this inner forest edge is tera, Pieridae) differ in habitat preferences? Biologia 58:943–951 the only egg-laying, nectaring (observations in this study) Berger D, Olofsson M, Gotthard K, Wiklund C, Friberg M (2012) and larval habitat of the species in otherwise too shady tree Ecological constraints on female fitness in a phytophagus insect. Am Nat 180:464–480 stands. (4) As males often settle on damp soil to absorb Cˇ elik T, Verovnik R, Gomboc S, Lasan M (2005) Natura 2000 v minerals (Lorkovic´ 1975; Benesˇ et al. 2002), it is reason- Sloveniji: Metulji (Lepidoptera). Zalozˇba ZRC SAZU, ZRC able to prevent asphalting of forest roads in species habi- SAZU tats. (5) In Slovenia, beech and some oak-hornbeam forests Chew FS, Robbins RK (1989) Egg-laying in butterflies. In: Vane- Wright RI, Ackery PR (eds) The biology of butterflies. Princeton have been managed as high forests for the last 50 years University Press, Princeton, pp 65–79 (Rozenbergar and Diaci 2003). This management includes Davies ZG, Wilson RJ, Coles S, Thomas CD (2006) Changing habitat two prevailing techniques, advanced group selection sys- associations of a thermally constrained species, the silver-spotted tem (non-uniform cutting on area 0.5 ha) and irregular skipper butterfly, in response to climate warning. J Anim Ecol 75:247–256 shelterwood system (Rozenbergar and Diaci 2003; Diaci Dennis RLH (2003) Towards a functional resource-based concept for 2006). In Illyrian oak-hornbeam forests (SE Slovenia), habitat: a butterfly biology viewpoint. Oikos 102:417–426 traditional coppicing and single tree selection system have Dennis RLH, Shreeve TG, Van Dyck H (2006) Habitats and been preserved only in the smaller remnants of former resources: the need for a resource-based definition to conserve butterflies. Biodivers Conserv 15:1943–1966 forest in agricultural landscape (Zavod za gozdove Diaci J (2006) Gojenje gozdov: pragozdovi, sestoji, zvrsti, nacˇrto- Slovenije 2011c). On the basis of the above, forest man- vanje, izbrana poglavja. Univerza v Ljubljani, Oddelek za agement suitable for L. morsei in the future should include gozdarstvo in obnovljive vire, Ljubljana the formation of a spatially and temporarily dynamic Fartmann T, Timmermann K (2006) Where to find the eggs and how to manage the breeding sites of the Brown Hairstreak (Thecla mosaic of greater canopy openness/gaps in high beech and betulae (Linnaeus, 1758)) in Central Europe? 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