View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by University of Debrecen Electronic Archive Insect Conservation and Diversity (2019) doi: 10.1111/icad.12369 SPECIAL ISSUE ARTICLE Changes in host ant communities of Alcon Blue butterflies in abandoned mountain hay meadows ANDRÁS TARTALLY,1 DAVID R. NASH,2 ZOLTÁN VARGA1 and 3 SZABOLCS LENGYEL 1Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary, 2Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark and 3GINOP Sustainable Ecosystems Group, Department of Tisza Research, Danube Research Institute, Centre for Ecological Research, Hungarian Academy of Sciences, Debrecen, Hungary Abstract. 1. Land use intensification is a general threat to biodiversity, but many species depend on low-intensity agricultural ecosystems. One example is European mountain meadow ecosystems, traditionally managed by hay harvesting or livestock grazing. Abandoning management often causes population declines, local extinctions and biotic homogenisation in these meadows. 2. We studied changes in the Myrmica host ant communities of the xerophilic form of the ant-parasitic Alcon Blue butterfly(Maculinea alcon) in four hay meadows in the Bükk mountains of Hungary between 2000–2007 and 2018. Abandonment started in this region in the 1970s, accelerated in the 1980s, and culminated in the 1990s. 3. We found that the Myrmica ant community has changed substantially in less than two decades. Diversity of the ant community always decreased, and species composition became more homogeneous at two sites. Habitat suitability for Maculinea butterflies decreased at three sites and increased at only one site, where management was restarted 20 years after abandonment. 4. The number of M. alcon caterpillars and pupae, the rate of infestation of ant nests and the mean number of caterpillars and pupae per ant nest decreased between the two periods, whereas host ant specificity did not differ from random in either period. 5. We conclude that the unfavourable changes in the host ant community due to aban- donment have negative consequences for the persistence of Maculinea populations. Our study highlights the need for detailed monitoring, and the maintenance of low-intensity management by mowing or grazing to avoid the decline of biodiversity dependent on low-intensity agriculture. Key words. Carpathian Basin, management, multiple host ant use, myrmecophily, Phengaris, social parasite, succession. Introduction (Kleijn et al., 2009). Mountain hay meadows and pastures are prime examples of human-maintained habitat types in land- Land use change is one of the major drivers of biodiversity loss scapes dominated by forests. These open habitats host unique in Europe (Rounsevell et al., 2018). In most of Europe, intensifi- plant and animal species that are characteristic of both lowland cation of land use, for example, increased inputs of chemicals in steppes and mountain meadows or grasslands, leading to the for- agriculture, is associated with negative impacts on the biodiver- mation of highly diverse communities packed with species of sity of natural habitats. However, many species and habitats have biogeographic and conservation importance. For example, adapted to long-term low-intensity farming, and farmland biodi- mountain hay meadows in Transylvania, Romania hold the versity has also declined considerably in the last few decades world record for plant species richness in 0.1 m2 and 10 m2 areas (Wilson et al., 2012). These meadows have been maintained for Correspondence: András Tartally, Department of Evolutionary Zool- centuries by regular human use, for example, for harvesting hay ogy and Human Biology, University of Debrecen, H-4032, Egyetem or livestock grazing, which effectively prevented the overgrowth tér 1, Debrecen, Hungary. E-mail: [email protected] of these open habitats by woody plants such as shrubs and trees © 2019 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological 1 Society This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 2 András Tartally et al. (Vera, 2000). The cessation of traditional land use often results all the available Myrmica species are suitable hosts of a given in succession starting with the appearance of woody plants, lead- M. alcon population (Thomas et al., 1989). Some Myrmica spe- ing to scrub, then patchy woodland and eventually to closed for- cies, for example, usually kill the caterpillars after adoption, est (Baur et al., 2006). In central and eastern Europe, the number especially under food stress (Elmes et al., 2004; Thomas et al., of grazing livestock started to decrease in the 1970s and 1980s 2005). This life cycle makes Maculinea butterflies highly sensi- and fell drastically in the 1990s due to socioeconomic changes tive to changes in the local Myrmica community. The Myrmica and changes in agricultural practices (Prokopová et al., 2018), communities in turn are sensitive to changes in their microhabi- leading to large-scale abandonment of mountain meadows. As tats (Elmes et al., 1998). Therefore, successional changes and/or a result, the vegetation and invertebrate fauna of mountain hay inappropriate management of a site can cause the decline of the meadows have changed considerably since the 1990s (Baur local host ant species, which in turn can result in the local extinc- et al., 2006). The maintenance of the biodiversity of these tion of the Maculinea population (Thomas, 1980; Thomas et al., unique, human-maintained habitat types thus requires active 2009). For these reasons, Maculinea butterflies are widely recog- management to halt succession and to keep them in their high- nised as indicator and umbrella species of their habitats (Settele diversity state (Stoate et al., 2009). et al., 2005), and are protected in most countries of Europe In many parts of Europe, Maculinea (= Phengaris) butterflies (Munguira & Martín, 1999). (Lepidoptera: Lycaenidae) are flagship species due to their com- Understanding the links between land use or management and plex life cycle and sensitivity to the status of their habitats Myrmica ant communities is thus of fundamental importance in (Settele et al., 2005). Mountain meadows and semi-dry grass- the conservation of species-rich mountain hay meadows and pas- lands in central Europe are often inhabited by the xerophilous tures, as well as the persistence of Maculinea butterflies. In addi- form of the Alcon Blue butterfly(Maculinea alcon [Denis & tion, study of the host ant specificity of Maculinea butterflies Schiffermüller], 1775), which we will refer to as M. alcon X also has evolutionary relevance. Following the pioneering work (Tartally et al., 2019). This butterfly has an unusual life cycle of Thomas et al. (1989), we have obtained extensive information in which the caterpillars start their development by feeding on on the host ant use of Maculinea butterflies in different regions of the developing seeds of gentian plants. In the final instar, the cat- Europe (Tartally et al., 2019), largely as a result of the MacMan erpillars are taken into their nests by Myrmica (Hymenoptera: collaborative research programme (Settele et al., 2002). These Formicidae) ants, and are raised together with the host brood insights (Tartally et al., 2019) aptly demonstrate the spatial (Thomas et al., 1989) for 1 or 2 years (Thomas et al., 1998a). dimension of the geographic mosaic of coevolution hypothesis The caterpillars mimic the odour (Schönrogge et al., 2004; (Thompson, 1999) in the Maculinea–Myrmica coevolved sys- Thomas et al., 2013) and the sound (Barbero et al., 2009) of tem. However, to our knowledge, the temporal dimension, that the ants and are mostly fed by the Myrmica workers by trophal- is, the dynamics of this system in time has not yet been suffi- laxis (Thomas & Elmes, 1998), although they also prey directly ciently addressed. on the ants’ brood (Tartally, 2004). A multitude of studies sug- The aim of this study was to evaluate whether and how gest that different Alcon Blue populations have adapted to differ- changes in land use and management influence Myrmica ant ent Myrmica species as their local hosts (Tartally et al., 2019). communities and their infestation by M. alcon X caterpillars There are both multiple-host-ant using populations, typically in and pupae in four meadows in the Bükk-mountains of northern central Europe, and more host-specific populations, typically in Hungary. Because many of the former mountain hay meadows western Europe (Tartally et al., 2019). The hygrophilic form of and pastures have already disappeared due to land abandonment, M. alcon (see ‘Study sites and populations’ below) uses mainly lack of management and shrub encroachment, it was not possible M. rubra and M. ruginodis in the north-west of Europe, and to obtain an adequate sample size to systematically examine dif- mainly M. scabrinodis and its close relatives in the remainder ferent management histories. Instead, we use the four study sites of Europe. M. alcon X generally exploits M. sabuleti or as case studies of different management histories. Traditional M. schencki and has a more diverse host ant usage in central land use was abandoned at different times at these four sites Europe than in the western or northern periphery