J Insect Conserv (2013) 17:1221–1228 DOI 10.1007/s10841-013-9603-7

ORIGINAL PAPER

Within-patch mobility and flight morphology reflect resource use and dispersal potential in the dryad butterfly Minois dryas

Konrad Kalarus • Piotr Sko´rka • Wiktor Halecki • Agata Jirak • Joanna Kajzer-Bonk • Piotr Nowicki

Received: 28 May 2013 / Accepted: 4 October 2013 / Published online: 25 October 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com

Abstract Knowledge of mobility is essential for under- resource availability rather than by recent evolutionary his- standing animal habitat use and dispersal potential, espe- tory. Lower female mobility may have negative implications cially in the case of species occurring in fragmented habitats. for the metapopulation persistence because only mated We compared within-patch movement distances, turning females are able to (re)colonise vacant habitat patches effi- angles, resting times, and flight-related morphological traits ciently. Conservation efforts should thus be focused on in the locally endangered butterfly, the dryad (Minois dryas), maintaining large habitat patches that prevent stochastic between its old populations occupying xerothermic grass- local extinctions. Furthermore, the recommendation of pro- lands and newly established ones in wet meadows. We moting the exchange of individuals among patches through expected that the latter group should be more mobile. Indi- improving matrix permeability, as well as assisted reintro- viduals living in both habitat types did not differ in their body ductions of the species into suitable vacant habitats should mass and size, but those from xerothermic grasslands had also improve its conservation. wider thoraxes and longer wings, thus lower wing loading index (defined as body mass to wing length ratio). The Keywords Endangered species Á Metapopulation Á majority of movements were short and did not exceed 10 m. Morphometric measurements Á Mosaic landscape Á Movement distances were significantly larger in males. Phenotypic plasticity However, there was no direct effect of habitat type on movement distances. Our results suggest that the dryads from xerothermic grasslands have better flight capabilities, Introduction whereas those from wet meadows are likely to invest more in reproduction. This implies that mobility is shaped by For most animals, mobility is a crucial trait that allows them to find basic resources such as mating partners, food or shelter. Moreover, mobility enables many animals to K. Kalarus (&) Á J. Kajzer-Bonk Á P. Nowicki persist in increasingly fragmented and heavily altered Institute of Environmental Sciences, Jagiellonian University, environments in which more and more species are forced to Gronostajowa 7, 30-387 Krako´w, Poland live (Fahrig 2003; Foley et al. 2005; Concepcion et al. e-mail: [email protected] 2008). Due to such environmental changes individuals P. Sko´rka must be able to reach habitat patches with the essential Institute of Zoology, Poznan´ University of Life Sciences, resources in order to survive (Fahrig 2003; Thomas et al. Wojska Polskiego 71 C, 60-625 Poznan´, Poland 2004; Dover and Settele 2009). Within-patch mobility W. Halecki enhances local population resilience to the habitat distur- Faculty of Environmental Engineering and Land Surveying, bance and may also be an indication of the potential University of Agriculture, Al. Mickiewicza 24/28, 30-059 exchange of individuals between local populations which Krako´w, Poland supports metapopulation persistence (Hanski and Ovas- A. Jirak kainen 2000; Kraus et al. 2003). Individuals with large Sa˛spo´w 334, 32-048 Jerzmanowice, Poland mobility may potentially explore all available resources 123 1222 J Insect Conserv (2013) 17:1221–1228 within a habitat patch as well as utilise those that are selected for the study. Two of them are xerothermic grasslands: widespread in different habitats (Dennis et al. 2003; Skołczanka (site A, 1.01 ha) and Uroczysko Kowadza (site B, Auckland et al. 2004; Kalarus et al. 2013). 0.72 ha). The other two are nearby wet meadows (site C, Several insect studies revealed that flight performance is 4.41 ha; site D, 1.04 ha). The inter-patch distances within the strongly associated with morphological traits (Berwaerts et al. pairs of patches of the same type are 80 m (for wet meadows) 2002; Merckx and Van Dyck 2002). For instance, it was found to 180 m (for xerothermic grasslands), whereas both pairs lie that butterflies from newly established populations have 200–400 apart. All the investigated sites are located within the longer wings (Merckx and Van Dyck 2002) and are charac- Bielan´sko-Tyniecki Landscape Park and are part of the Natura terized by increased mobility (Hanski et al. 2006). However, it 2000 site ‘‘De˛bnicko-Tyniecki Obszar Ła˛kowy’’ (PLH remains unknown if morphological traits are also related to 120065). A more detailed description of all four study sites can mobility at a very local, within-habitat patch scale. be found elsewhere (Kalarus et al. 2013). Knowledge of mobility is especially important in the case We examined within-patch movements by the dryads, of endangered species occurring in small and isolated local their resting times between consecutive flights, and mor- populations, which are surrounded by an inhospitable matrix phological traits potentially related to mobility. The (Mathias et al. 2001;Thomasetal.2001; WallisDeVries movements were recorded from the moment when a spot- 2004). One such species is a specialist butterfly, the dryad ted butterfly was initially noticed resting on a plant. But- Minois dryas (Scopoli 1763). In Poland, the occurrence of terflies were followed by observers from the distance of this species is restricted to few isolated localities in the south about 5 meters in order to avoid disturbing butterflies. of the country, including the Krako´w region, where it sur- Points where the butterfly stopped were subsequently vives in protected calcareous xerothermic grasslands, and marked with numbered bamboo poles. This made it pos- more recently has spread into surrounding wet meadows sible to measure distances of movements and turning (Da˛browski 1999; Kalarus et al. 2013). Therefore, it is worth angles between them with the help of steel measuring tape to examine whether the dryads living in wet meadows differ and compass. Resting time between consecutive move- in mobility and flight morphology from those inhabiting ments was recorded with the precision of one second. Other xerothermic grasslands. It can be expected that the indi- types of behaviour were very rarely observed and thus were viduals from former group should be more mobile and cover not considered in the present study. After the fifth con- longer distances, which should also be reflected in their secutive movement the butterfly was captured with an morphology since they are the descendants of the most entomological net. Thorax width and forewing length were dispersive butterflies and their mobility is likely to possess a then measured to the nearest 0.1 mm using a Vernier cal- substantial genetic component (Hill et al. 1999;Merckx liper. Finally, each individual was placed in a small et al. 2003;Haagetal.2005). envelope and weighted with a TOMOPOL S-50 balance The aim of our study was to investigate differences in with the precision of 0.005 g. The weighting was repeated within-patch movements and flight morphology between twice for each butterfly and averaged. Having taken all the the dryads from xerothermic and wet habitats. In addition, above measurements, we marked the butterfly with a we focused on inter-sexual differences in mobility, which unique number on the underside of its hind wing with a are typically strong in butterflies, but often neglected non-toxic permanent marker, and immediately released it. (Ovaskainen et al. 2008; Nowicki and Vrabec 2011; The data from any individual (even if recaptured) were Schultz et al. 2012). Specifically, for both habitat types and used only once in the analyses to avoid pseudoreplication. sexes we compared (1) movement distances and turning angles; (2) morphological traits possibly associated with Statistical analysis butterfly mobility (body mass, forewing length, thorax width, wing loading index, and general body size index); Since our survey design was incomplete, i.e. not every site (3) resting times, which are inversely related to flight was surveyed in both years of the study; we were not able activity. Based on the results obtained we also provide to test the effects of site and year separately. Thus, we practical conservation recommendations for the dryad. instead adopted the effect of a data set, i.e. data collected at a given site in a particular year, as a random factor in the analyses conducted using generalized linear mixed models Methods (GLMMs) with parameter estimates derived using the restricted maximum likelihood (REML) method (Searle Fieldwork et al. 1992; Wolfinger et al. 1994). The data set effect was always nested within habitat type. Nevertheless, in all the The survey was carried outduring theflightperiod ofthedryad, cases, it proved insignificant and did not improve the i.e. August, in 2009 and 2010. Four habitat patches were model fit. Consequently, with this effect removed, the final 123 J Insect Conserv (2013) 17:1221–1228 1223 models were reduced to standard general linear models U2 test (Zar 1998) was applied to examine whether the (GLMs). distributions were consistent with the von Mises distribu- Separate GLMs were applied to test the impacts of tion. We also calculated the concentration index K (Fisher habitat type and sex as well as their interaction term on the and Best 1979) of the turning angle distribution for each morphological characteristics of the dryads. The investi- habitat type to obtain how the distributions are concen- gated traits included body mass, thorax width, forewing trated around the mean angle. The concentration index K is length, wing loading index, and general body size (see a measure of the deviation of the angle distribution from a below). The traits were derived for the purpose of sub- uniform one (Mardia and Jupp 2000). Higher K index sequent analyses as the original traits were clearly posi- values indicate higher concentration of angle distribution. tively correlated with one another (ln-transformed body The GLMs were calculated in JMP 10, while the turning mass vs. thorax width: r = 0.489, P \ 0.001; ln-trans- angle analysis was done in the Oriana 3.0 software. formed body mass vs. wing length: r = 0.602, P \ 0.001; thorax width vs. wing length: r = 0.589, P \ 0.001). Wing loading index was defined as the ratio of body mass to Results forewing length. Applying the classic definition of wing loading (i.e. body mass to wing surface ratio; see Dudley The GLM models for morphological traits indicated strong and Srygley 1994) was not possible, because wing surface inter-sexual differences in each case (Table 1). Females of measurements could not be easily taken in the field, and the dryad were heavier, had wider thorax and longer wings, thus we had to rely on a proxy using wing length instead (as e.g. Tiple et al. 2009). General body size index was Table 1 Results of the GLM model analysis of factors affecting calculated as the sum of standardised values of body mass, flight-related morphological traits of the dryad thorax width and wing length obtained through dividing the Variable Effect Df F R2 P measurements by the means for all individuals. Body mass measurements were cubic rooted before standardisation. Body mass Model fit 1 38.797 0.499 0.001 We decided to rely on the derived index rather than to use Habitat type 2.79 0.098 body mass as a measure of body size, because butterfly Sex 1 115.78 0.001 body mass varies (typically decreases) during adult life Habitat 1 1.357 0.246 span, and definitely we were not able to weight all indi- type 9 sex viduals in the same moment of their life, e.g. directly after Error 111 hatching. Thorax width Model fit 1 20.412 0.338 0.001 In the next step, further GLMs were built to explain Habitat type 6.312 0.013 patterns in the average movement distances and resting Sex 1 49.29 0.001 times. The latter was used as a measure of butterfly inac- Habitat 1 3.74 0.056 tivity. Both variables were ln-transformed to achieve their type 9 sex normal distribution. Among the predictors the models Error 111 included butterfly sex, habitat type and their interaction Wing length Model fit 1 34.667 0.47 0.001 term as fixed effects; as well as wing loading and butterfly Habitat type 4.193 0.043 size indexes as continuous covariates. Sex 1 93.696 0.001 Turning angles were grouped into twelve 30°-wide Habitat 1 3.926 0.05 classes. Their distributions were first tested for inter-sexual type 9 sex differences separately for xerothermic grasslands and wet Error 111 meadows with Chi square tests. Since there were no sig- Wing loading Model fit 1 23.361 0.373 0.001 index nificant differences in any case, the data for both sexes Habitat type 5.102 0.026 were pooled together for further analyses of the turning Sex 1 67.972 0.001 angle distributions. The distributions were compared Habitat 1 0.815 0.368 type 9 sex between the two habitat types, again using Chi square test. Error 110 Additionally, the distributions for each habitat type were evaluated against two theoretical distributions: the uniform Body size index Model fit 1 53.323 0.584 0.001 distribution and the von Mises distribution, which is Habitat type 1.688 0.197 equivalent to the normal distribution for circular data Sex 1 151.42 0.001 (Fisher and Best 1979; Batschelet 1981). The uniformity of Habitat 1 4.828 0.03 type 9 sex the turning angle distributions was assessed with the Rao’s Error 109 spacing test (Mardia and Jupp 2000), whereas the Watson’s 123 1224 J Insect Conserv (2013) 17:1221–1228 but males had lower wing loading index (Fig. 1). Fur- In general, females tended to rest longer than males thermore these inter-sexual differences were clearly con- (Tables 2, 4). Although habitat type alone did not affect the firmed for body size index in the interaction term habitat resting times of butterflies, its interaction with sex was type 9 sex (Fig. 1). Individuals from xerothermic grass- lands proved to have longer wings and lower wing loading Table 3 Results of the GLM model analysis of factors affecting index than those from wet meadows (Table 1; Fig. 1). In average movement distances of the dryad butterflies addition, the thorax was significantly wider in the former Df F R2 P group, but the difference was evident only in males. For Effect better illustration of morphometric measurements of the Model fit 4.456 0.134 0.001 dryad butterflies their mean values are shown in Table 2. Habitat type 1 0.081 0.777 The analysis of distances covered by the dryads revealed Sex 1 18.894 0.001 a significant effect of sex, with males flying further dis- Habitat type 9 sex 1 1.293 0.258 tances than females, but not of habitat type (Tables 2, 3; Wing loading index 1 0.666 0.416 Fig. 2). The majority of movement distances were quite Body size index 1 1.863 0.175 short ([10 m) and very few exceeded 20 m, especially in Error 107 females (Fig. 2).

Fig. 1 Morphological traits (mean ± SE) of the dryad butterflies in both investigated habitat types. White and grey bars represent females and males respectively

Table 2 Morphological traits and movement characteristics (mean ± SE) of the investigated dryad butterflies in relation to their sex and habitat type Traits of the dryad Sex Habitat type Female Male Xerothermic Wet

Body mass [mg] 153.7 ± 4.68 90.9 ± 3.73 125.5 ± 5.48 131.1 ± 6.79 Thorax width [mm] 3.90 ± 0.052 3.30 ± 0.070 3.77 ± 0.068 3.52 ± 0.069 Wing length [mm] 30.10 ± 0.234 26.65 ± 0.267 29.15 ± 0.302 28.10 ± 0.363 Movement distance [m] 5.96 ± 0.428 7.99 ± 0.498 6.84 ± 0.441 6.73 ± 0.521 Resting time [s] 61.6 ± 9.01 30.9 ± 8.05 50.2 ± 8.33 47.5 ± 9.97

123 J Insect Conserv (2013) 17:1221–1228 1225

Fig. 2 Distribution of within-patch movement distances of the Fig. 4 Inter-sexual differences in resting times (mean ± SE) of the dryads. White and grey bars represent females (n = 75) and males dryad in both investigated habitats. White and grey bars represent (n = 52) respectively. To avoid psedoreplication a single movement females and males respectively. To account for the significant per individual was randomly selected for the histogram relationship between butterfly wing loading index and resting time, the values presented are residuals of this relationship Table 4 Results of the GLM model analysis of factors affecting average resting times of the dryad butterflies Df F R2 P habitat, while there was no particular difference between resting times of both sexes in xerothermic grasslands Effect (Fig. 4). Model fit 1 7.110 0.214 0.001 Distributions of turning angles did not differ between Habitat type 0.783 0.378 sexes in any habitat (xerothermic grasslands: v2 = 4.251, Sex 1 8.830 0.004 P = 0.962; wet meadows: v2 = 5.700, P = 0.893). How- Habitat type 9 sex 1 10.455 0.002 ever, with the data for both sexes pooled together, they did Wing loading index 1 7.098 0.009 so between both habitats (v2 = 21.281, P = 0.031; Fig. 5). Body size index 1 3.494 0.064 Furthermore, the Rao’s spacing test outcome showed that Error 107 the distributions were clearly not uniform, but instead they were consistent with the von Mises distribution as sug- gested by the insignificant Watson’s U2 test results (Table 5). In both habitat types the great majority of turning angles were centred near 0 (Fig. 5; see also rela- tively high values of the concentration index K in Table 5), which indicates that butterflies tended to move in fairly straight lines without much change in the flight direction.

Discussion

Numerous earlier studies have documented the relationship between morphological traits of various butterfly species and their mobility. Specifically, it has been found that mobility is negatively affected by body mass, but positively Fig. 3 Relationship between wing loading index and resting time of by thorax width and wing length (Berwaerts et al. 2002; the dryads Sko´rka et al. 2013). The results of the present study gen- erally confirm the above patterns, although we found that highly significant (Table 4). The GLM model results also wing loading index is more useful as a factor explaining the implied a positive relationship between wing loading index dryad mobility. Wing loading index correlated positively, and resting time (Table 4; Fig. 3). With this relationship while body size index correlated negatively with resting accounted for, resting times were the longest in females time, but only the former relationship proved statistically from wet meadows and the shortest in males from the same significant. 123 1226 J Insect Conserv (2013) 17:1221–1228

Fig. 5 Distribution of turning angles of the dryad flights within their respective habitat patches (a xerothermic grasslands, b wet meadows). The solid lines indicate the mean angle (presented with 95 % confidence interval). The inner scale shows frequencies of turning angles within 30°- wide classes

Table 5 Comparisons of the dryad turning angles distributions in dryad mobility through its effect on flight-related mor- two investigated habitat types phology, we found no evidence for its additional direct Xerothermic grasslands Wet meadows influence on local mobility, although effects may be pres- ent on realized dispersal. Moreover, this indirect effect of N 284 224 habitat type was in the opposite direction than expected, Concentration index K 1.022 0.871 i.e. the individuals representing recently established pop- Rao’s spacing test ulations in wet meadows turned out to be less mobile. U 192.56 173.89 Consequently, it seems justified to hypothesise that P \0.01 \0.01 mobility and flight morphology of the dryad within the Watson’s test studied region is shaped by differences in resource avail- U2 0.068 0.042 ability among habitat patches as a result of phenotypic P 0.1 [ P [ 0.05 0.5 [ P [ 0.25 plasticity (cf. Merckx and Van Dyck 2006), rather than by Rao’s spacing test and Watson U2 test were applied to assess the the recent evolutionary history of the populations inhabit- consistency with the uniform distribution and the von Mises one ing them. It is known, that availability and quality of respectively foodplants affect morphology of adult individuals (Fischer and Fiedler 2000). In earlier research on the dryad we have Comparisons of morphological characteristics between demonstrated that xerothermic grasslands offer substan- the two investigated habitat types indicated that the dryads tially more nectar sources, whereas wet meadows are from xerothermic grasslands appear more adapted to flight. generally better in terms of larval foodplant abundance They had wider thoraxes and longer wings than the indi- (Kalarus et al. 2013). Since nectar is the predominant viduals from wet meadows, and consequently, lower wing source of energy utilised for flight by many butterfly spe- loading index, since there was no difference in body mass cies (Sacktor 1975; Kammer and Heinrich 1978), its between both groups. Nevertheless, despite apparently increased availability supports highly mobile individuals. greater potential mobility of the butterflies inhabiting In contrast, the dryads living in wet meadows are likely to xerothermic grasslands, habitat type alone had no apparent invest more in reproduction. It is worth noting that thinner impact on within-patch movement distances. However, thoraxes recorded in this habitat apparently imply larger these morphological differences may indicate that dryads abdomens, as body mass did not differ between both from xerothermic grasslands are more capable to success- grassland types. Greater investment in reproduction pre- fully migrate from natal patches than butterflies from wet sumably leads to less investment in flight capacity since a meadows. trade-off between both investments should be expected There was no clear effect of habitat type on the resting (Gibbs and Van Dyck 2010). times. Females from wet meadows rested longer, but males The flight distances of the dryads within their habitat rested shorter than the butterflies from xerothermic grass- patches were strikingly short in most cases. The movement lands. In wet meadows, relatively long resting times in distances recorded in our study were not only well below females may force males to take flight more frequently in distances separating habitat patches, but also considerably order to search for mating partners. Taking everything into shorter than patch dimensions. In addition, the fact that consideration, while habitat type indirectly affected the turning angles fitted well with the von Mises distribution

123 J Insect Conserv (2013) 17:1221–1228 1227 indicates that the flight routine followed correlated random funds as well as by the Bratniak Foundation. The authors are grateful walk (Kareiva and Shigesada 1983). Altogether our find- to the students of the Jagiellonian University and the volunteers, especially Katarzyna Czober and Jakub Osika who participated in the ings suggest limitations to the dryad movements within fieldwork. We also thank Bernard Kromka for improving the English their patches (cf. Hovestadt and Nowicki 2008). in the manuscript. Mobility depression in highly fragmented landscapes has been frequently reported in butterflies (Mathias et al. Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, dis- 2001; Hanski and Meyke 2005; Bergerot et al. 2012). The tribution, and reproduction in any medium, provided the original phenomenon has serious conservation implications as it author(s) and the source are credited. decreases metapopulation viability (Hanski 1999; Russell et al. 2006). In our study system, the situation may be worsened by male-biased mobility. While females are often References a more mobile sex in butterflies (e.g. Bergman and Landin 2002; Auckland et al. 2004; Nowicki and Vrabec 2011,but Auckland JN, Debinski DM, Clark RW (2004) Survival, movement, see Junker and Schmitt 2010), we observed the opposite and resource use of the butterfly Parnassius clodius. Ecol Entomol 29:139–149 pattern in the dryad. This is a further constraint for the Batschelet E (1981) Circular statistics in biology. Academic, New successful conservation of this species because only mated York females are able to ensure colonisations of vacant habitat Bergerot B, Merckx T, Van Dyck H, Baguette M (2012) Habitat patches, which is a key process for metapopulation per- fragmentation impacts mobility in a common and widespread woodland butterfly: do sexes respond differently? BMC Ecol sistence. It is also possible that low, male-biased mobility 12(1):5 has led to the extinction of the dryad in northern Poland as Bergman KO, Landin J (2002) Population structure and movements was earlier reported (Romaniszyn and Schille 1929; of a threatened butterfly (Lopinga achine) in a fragmented Da˛browski 1994); as well as to its decline in Germany landscape in Sweden. Biol Conserv 108:361–369 Berwaerts K, Van Dyck H, Aerts P (2002) Does flight morphology (Settele et al. 1999). relate to flight performance? An experimental test with the Because the distances covered by the dryad are so low, butterfly Pararge aegeria. Funct Ecol 16(4):484–491 the colonisation of empty patches may be difficult. The Buszko J, Masłowski J (2008) Motyle Dzienne Polski. Koliber, Nowy recommended conservation actions should be focused on Sa˛cz Concepcion ED, Diaz M, Baquero RA (2008) Effects of landscape enhancing the chances of continuous existence of local complexity on the ecological effectiveness of agri-environment populations despite presumably low exchange of individ- schemes. Landscape Ecol 23:135–148 uals. This should be achieved through maintaining rela- Da˛browski JS (1994) Successful attempts of reintroduction of local tively large habitat patches, which should prevent populations of Lepidoptera from the species Zygaena carniolica (Zygaenidae) and Minois dryas (Satyridae) into protected areas stochastic extinctions of their populations (Hanski 1999). of the southern Poland. 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Appl Stat 28:152–157 recent years, proved to be particularly successful in Foley JA, De Fries R, Asner GP, Barford C, Bonan G, Carpenter SR, establishing new viable populations (Da˛browski 1994). Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Acknowledgments The study was funded by the Polish National Prentice IC, Ramankutty N, Snyder PK (2005) Global conse- Science Centre Grant No. N304 064139 and by the German Federal quences of land use. Science 309:570–574 Ministry of Education and Research under its FP6 BiodivERsA Gibbs M, Van Dyck H (2010) Butterfly flight activity affects Eranet project CLIMIT. The fieldwork was additionally supported by reproductive performance and longevity relative to landscape the Jagiellonian University through its DS/WBINOZ/INOS´/761/09-10 structure. Oecologia 163(2):341–350 123 1228 J Insect Conserv (2013) 17:1221–1228

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