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Lepidoptera: Nymphalidae) EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 113: 104–112, 2016 http://www.eje.cz doi: 10.14411/eje.2016.013 ORIGINAL ARTICLE Climate-induced changes in the phenotypic plasticity of the Heath Fritillary, Melitaea athalia (Lepidoptera: Nymphalidae) EDIT JUHÁSZ 1, ZSOLT VÉGVÁRI 2, JÁNOS P. TÓTH 3, KATALIN PECSENYE 1 and ZOLTÁN VARGA1 1 Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, Debrecen 4032, Hungary; e-mails: [email protected], [email protected], [email protected] 2 Department of Conservation Zoology, Hortobágy National Park Directorate, University of Debrecen, Sumen u. 2, Debrecen 4024, Hungary; e-mail: [email protected] 3 MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Egyetem tér 1, Debrecen 4032, Hungary; e-mail: [email protected] Key words. Lepidoptera, Nymphalidae, Melitaea athalia, butterfl y, Carpathian Basin, morphology, Procrustes anova Abstract. Recently a large number of studies have reported an increase in the variability in the climate, which affects behavioural and physiological adaptations in a broad range of organisms. Specifi cally, insects may be especially sensitive to climatic fl uctua- tions, as their physiology and life history traits, like those of other ectotherms, are predominantly affected by environmental factors. Here we aimed to investigate climate-induced changes in several morphometric measures of the Heath Fritillary in North-Eastern Hungary, which is a highly diverse transitional area. During this study we tested the following hypotheses: (i) climate affects genitalia and body size to various degrees (ii) increasing variability in climate induces higher levels of fl uctuating asymmetry and variance in all morphological characters. To our knowledge, this study is the fi rst to analyse simultaneously wing size and structure of genitalia of a butterfl y in response to variability in climate. Our fi ndings suggest that wing and genital traits may exhibit similar degrees of stability in response to a more variable climate, although the response in terms of forewing size differs from that of other body measurements and the structure of the genitalia. These fi ndings suggest that global climate change may affect lepidopteran body metrics over longer periods of time. Our fi ndings parallel the results of investigations showing that insect morphology might be modifi ed by environmental changes, which is especially the case for those body parts that are phenotypically very variable. However, we found no evidence that increasing variability in climate would induce higher levels of fl uctuating asymmetry and greater variability in morphological characters. INTRODUCTION Characteristics of butterfl y wings are widely used as Evidence is accumulating that most habitat loss, frag- model system for studying development or phenotypic mentation and long-term changes in climate can be attrib- plasticity (Dennis & Shreeve, 1989; Berwaerts et al., 1998; uted to anthropogenic factors (Bellard et al., 2012; Man- Hill et al., 1999; Thomas & Van Dyck, 2006; Talloen et tyka-Pringle et al., 2012). It is of particular interest to know al., 2009; Gibbs et al., 2011). For example, coloration and how different organisms react to changes in climate and patterns on the wings of some species of butterfl ies are weather over long periods of time, especially in terms of known to be very variable and show high levels of pheno- their phenology and morphological adaptations. Specifi - typic plasticity in response to different environmental fac- cally, insects may be especially sensitive to fl uctuations in tors (Shapiro, 1976; Brakefi eld et al., 1996; Brakefi eld & climate, as their physiology and life history traits are pre- French, 1999; Talloen et al., 2009) or food quality (Kooi dominantly affected by environmental factors as are those et al., 1996). Specifi cally, human-induced habitat frag- of other small ectotherms (Bale et al., 2002; Wilson et al., mentation has been shown to drive morphological modi- 2007). Thus, variation in food availability, predation pres- fi cations (Berwaerts et al., 1998). Furthermore, results of sure, temperature, length of the season, photoperiod and experimental studies support the hypothesis that changes humidity can affect the responses of organisms (Hughes et in climate drive morphological characters (Gibbs et al., al., 2003, 2007; Karlsson & Van Dyck, 2005). Heterogene- 2011): Xi et al. (2015) indicate that temperature increase ous environments provide opportunities for exploring the per se and its interaction with the direction of temperature role and limits of natural selection in shaping the response change should be primarily responsible for shifts in body of organisms to environmental change (Pigliucci, 2001). size at different times of the year. Therefore, seasonal pat- terns in temperature in temperate regions could be of gen- Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 104 Juhász et al., Eur. J. Entomol. 113: 104–112, 2016 doi: 10.14411/eje.2016.013 eral importance for predicting changes in animal body size strained genetic control than body metrics, therefore we in respone to a warmer climate. In contrast, insect genital expect that changes in temperature will affect genitalia and characteristics differ greatly, even between sibling species, body measurements differently. Thirdly, we aim to test the and seem to be only slightly affected by environmental fac- hypothesis that with increase in climatic variability there tors (Cesaroni et al., 1994; Dapporto et al., 2009, 2011). is an increase in fl uctuating asymmetry and variance in all As a result of environmental perturbations, self-regu- morphological characters (Joubert & Bijlsma, 2010). latory mechanisms might be unable to stabilize develop- MATERIALS AND METHODS ment (Van Valen, 1962; Palmer & Strobeck, 1986, 1992). Fluctuating asymmetry, which consists of small random Climate data differences between left and right sides in bilaterally sym- We obtained meteorological data for 1967–2013 from the near- metrical structures of organisms, is a widely used meas- est meteorological station at Miskolc (48.1°N, 20.4°E), which is ure of developmental instability (Van Valen, 1962; Palmer, 60 km from the study site, and the only station for which there 1997). However, there is growing evidence from both ex- is long-term dataset necessary for determining trends in climate perimental and non-experimental studies that fl uctuating (Végvári et al., 2014). To assess temporal patterns in climatic pre- dictors relevant for larval development of the species studied, we asymmetry does not consistently predict stress or fi tness calculated (i) mean temperatures in March, April and May (ii) (Lens et al., 2002; Silva et al., 2009). temperature averaged across March to April and March to May Owing to their highly variable morphometric character- (iii) mean seasonal temperatures (iv) precipitation sums for the istics, members of the genus Melitaea (Lepidoptera: Nym- above periods, which is when the larvae are feeding. To calculate phalidae) provide opportunities for studying the effects of the same metrics for the pre-diapausal and diapausal periods, we climate change and variability on lepidopteran morpholo- repeated these analyses for July and August to February, respec- gy. In addition, butterfl ies are particularly well represented tively (Pöyry et al., 2011). Monthly and seasonal means of cli- in museum collections, thus morphometric studies can also matic proxies are widely used in insect studies (Altermatt, 2010a; be carried out on both wings and external genitalia of a Gibbs et al., 2011; Mega, 2014). Although climatic parameters may fl uctuate strongly within a month, we were interested in the number of lepidopterans using historical data. effects of the overall trend in climate. To detect temporal trends In the present study, we aim to investigate the effects of in weather proxies, we fi tted linear regressions to these variables changes in climate on the (i) wing size and (ii) genital char- as a function of years. acteristics of the Heath Fritillary butterfl y – Melitaea ath- Sample collection alia (Rottemburg, 1775), which is a threatened species in In total, 228 male individuals were analyzed all of which were Western Europe but not yet endangered in the eastern part captured in the Jósvafő area of the Aggtelek Karst region, East- of the continent (Van Swaay & Warren, 1999; Van Swaay Hungary. Specimens were collected between 1967–2013 only in et al., 2010). For example, this species is a priority species May and June and stored in the collection of the University of De- for butterfl y conservation in England, where its phenology brecen (Table 1). As only male individuals were available in suffi - and population structure have been studied in detail (War- ciently large numbers to carry out the analyses and morphometric ren, 1987a, b, c, 1991; Hodgson et al., 2009). In contrast, traits (measure and shape) showed marked sexual dimorphism, this species occurs in an astonishing variety of ecological we used only the data for male specimens. Further, to increase the situations in Hungary. The main object of the present work robustness of our results, we removed records for years when less is
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