vulnerable species in the world. All European Phengaris species belong to the most intensively studied group of butterflies in Eurasia. Five species are known in ...
EUROPE’S THREATENED SPECIES: THE CASE OF ENDANGERED PHENGARIS (MACULINEA) BUTTERFLIES (LEPIDOPTERA, LYCAENIDAE) Paula Seixas Arnaldo1,2, Maria da Conceição Rodrigues1,2, Teresa Fidalgo Fonseca1
1
University of Trás-os-Montes and Alto Douro, Forest Science and Landscape Architecture Department, 5001-801 Vila Real, Portugal 2 Center of the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes and Alto Douro, 5001-801 Vila Real, Portugal
Abstract The increasing fragmentation of landscapes and the degradation of suitable habitats are considered to be the greatest challenges to the conservation of Phengaris butterflies in Europe. Because of their remarkable life-cycle, including an obligatory relationship with ants, Phengaris butterflies require a very specific combination of ecological conditions and so have a narrow tolerance for environmental change. In this paper, we summarize our knowledge of the ecology and the conservation status of five highly endangered Phengaris butterflies: Phengaris arion, P. teleius, P. nausithous, P. rebeli and P. alcon. We discuss the current knowledge of their natural dynamics, the influence of habitat management, and procedures that could aid in the conservation of these endangered species.
Introduction Populations of many species of Lepidoptera are in decline all over Europe, due primarily to habitat destruction and fragmentation [1]. In recent decades, climate change has also affected the decline and spatial redistribution of many butterfly species [2-3] with an observed movement of species northwards [4-6]. Although many species are affected by such events, the genus Phengaris Doherty, 1891 [according to Fric et al, [7] is the senior synonym of Maculinea van Eeche, 1915], can be ranked amongst the most vulnerable species in the world. All European Phengaris species belong to the most intensively studied group of butterflies in Eurasia. Five species are known in Europe: Phengaris arion (Linnaeus, 1758), P. teleius (Bergsträsser, 1779), P. nausithous (Bergsträsser, 1779), P. alcon (Denis & Schiffermüller, 1775) and P. rebeli (Hirschke, 1904). The entire genus Phengaris, has suffered severe declines in Europe, and one species, P. arion (Linnaeus, 1758) became extinct in the Netherlands in the 1960s and in UK in the 1970s, until reintroduced [8-9]. The International Union for the Conservation of Nature (IUCN), labels P. arion, P. alcon and P. rebeli with a ‘vulnerable’ status, whereas P. teleius and P. nausithous are considered ‘threatened’ [10]. P. teleius and P. nausithous are included in Annexes II and IV of the European Habitats’ Directive, but P. arion is listed only in Annex IV.
Also, P. arion, P. teleius and P. nausithous are mentioned in the Berne Convention. According to Wynhoff [11], P. teleius is relatively the best protected species while P. rebeli is the least, probably due to its unclear taxonomic status. In the global scientific community, there is considerable controversy as to the taxonomic status of P. alcon and P. rebeli, with no genetic differentiation found between them [12-14]. However these authors have agreed that two ecologically different forms can be distinguished; P. alcon restricted to the wet heaths and moorlands with Gentiana pneumonanthe as host plant, whereas P. rebeli exclusively inhabits xerothermous grasslands on G. cruciata as host plant. Thus, although both species do not represent distinct evolutionarily significant units, they can be deemed as different targets for habitat conservation strategies [15].
The recent distribution of the European Phengaris species Geographically, the genus Phengaris, commonly named the “Large Blues”, is confined to the Palaearctic ecozone: ecoregions of Europe and Asia north of the Himalaya foothills. P. rebeli occurs only in Europe, but P. arion, P. teleius, P. nausithous, and P. alcon extend into Asia. A sixth species, P. arionides (Staudinger) occurs only in Asia (Japan, China, and South Korea). For all Phengaris species, the eastern boundaries of their range distribution are unclear, and there is little information on their distribution, status, or ecology, within nations of the former USSR or its neighbours. In Europe, Phengaris butterflies occur in 38 countries, always between the 38th and 62nd parallels, with northernmost populations in Finland and southernmost in Turkey [9]. Their status is deemed to be stable in only seven countries [1, 11]. Iceland, Ireland and Norway have no Phengaris species. Phengaris arion (Linnaeus, 1758) Distributed from the North of the Iberian Peninsula, present in most of Central Europe to Fennoscandia, eastwards to Mongolia. Throughout Europe, P. arion is endangered and is protected by the EU Habitat Directive. It was extinct from the Netherlands in 1964 and the UK in 1979, but was reintroduced into the UK in 1986 using a similar race from the island of Oland of the Sweden coast. It exists only in small local populations on the Swedish mainland [11]. Currently, only three populations are known from the South coast of Finland: one near Asikkala region and two in the southeast of the country. The latter occur near Lake Saimaa (South Karelia) and near Liperi (North Karelia), and are the northernmost European populations of P. arion. According to Kolev [16] the Finnish populations differ from Central European or Russian populations. In Denmark, many local populations of P. arion have been extirpated and only one small population in the east, as well as a couple of populations in northwestern Jutland, was still found [Stoltze, 1996 cit. by 17]. P. arion has also disappeared locally in Germany and Belgium. Populations of P. arion are rare in Hungary, Ukraine, Moldova, Lithuania and Slovenia. In the Czech Republic, a dense system of P. arion colonies inhabits remote valleys of the NW Carpathians [18]. In Poland, P. arion has disappeared from the western parts of the country but it is still widely distributed in the south and east [19]. Populations of P. arion are stable in Albania, Bulgaria, Switzerland, Estonia, France and Greece. In many other countries its status is unknown, including Liechtenstein, Croatia, Yugoslavia, Bosnia, Russia (European part) and Andorra [1]. Phengaris nausithous (Bergsträsser, 1779)
Euro-Siberian distribution in a wide range over Western and Central Europe to Kazakhstan, Southern Siberia and Mongolia [11, Lukhtanov and Lukhtanov, 1994, cit. by 20]. It occurs in the north of the Balkan Peninsula [21] and from northern Turkey [Hesselbarth et al, 1995, cit. by 20], but is very rare and local in eastern France, central Europe, Caucasus, central and southern Urals, and Altai. It is relatively widely distributed and locally frequent in the western, northern hilly, and lowland regions of the Carpathian basin (e.g. mostly in the areas bordering Austria, Slovenia and Hungary) but completely absent in the Pannonian lowland along and East of the river Danube [20]. It was recently discovered in Transylvania (Romania) [20]. In Germany there are still many populations, whereas in Spain P. nausithous only occurs in the north of Leon and near Madrid [22], but populations are considered stable. Populations in Bulgaria and Poland, are also stable but in Liechtenstein and European Russia their status is unknown [1]. Phengaris teleius (Bergsträsser, 1779) Very rare and locally distributed, often co-occurring with P. nausithous: found in Austria, Belgium, Croatia, Czech Republic, France, Georgia, Germany, Hungary, Italy, Japan, Kazakhstan, Mongolia, Poland, Russia, Serbia and Montenegro, Spain, Switzerland, and Ukraine. It has suffered a major decline all over Europe and is listed in Appendix II and IV of the EU Habitats Directive. In Bavaria (Germany), P. teleius is significantly rarer than its sister species P. nausithous, and is regarded as highly threatened and a species of concern. In the Netherlands, P. teleius populations were extirpated from the centre of the country, and later reintroduced [11]. In Russia, the status of P. teleius populations is unknown. Phengaris alcon (Denis & Schiffermüller, 1775) The second most widespread lycanid butterfly, with a scattered occurrence throughout Europe [11]. Present in the north of Portugal and Spain, France, most of central and parts of eastern and southern Europe, Asia Minor and through temperate Asia to east Siberia, Kazakhstan, Mongolia and Altai [9]. Northernmost populations occur in Sweden, and in Denmark where it is found only on the Jutland peninsula and adjacent islands (Læsø, Fanø and Rømø) [Stoltze, 1996, cit. by 17]. In Portugal, P. alcon is the only representative of the genus, occurring only in very local populations in the north [23], and similarly in Spain it is restricted to Cantabrica and the west of the Iberic Peninsula. In France, large populations are known from the Sarthe. The Netherlands has two populations, with most in the north [Tax, 1989, cit. by 11], and in nearby Belgium populations are found by the border [24]. In Germany, it is restricted to several regions but can be quite common [11], as also in northeast Austria, Slovenia and northern Croatia. Populations occur in the North of Hungary, Romania, Ukraine, Moldavia and Poland [1]. Phengaris rebeli (Hirschke, 1904) Has the most restricted range distribution, confined to Europe and to only 16 countries. Present on dry mountain meadows in northern Spain, in Italy, southeast Europe, and especially in the Massif Central of France, and the French Alps. In Bulgaria, Switzerland and Spain, populations are stable whereas it has been extirpated from Belgium. In Poland, P. rebeli was recorded for the first time in the Pieniny Mountains in 1987 [25] and was later discovered in the south-east [26-27]. It has been found recently in Lithuania [28]. According to van Swaay and Warren [1] its status is unclear in many countries because of taxonomical confusion with P. alcon.
Habitat and ecology of Phengaris species These species live on different vegetation types on comparatively poor soil. Thus, P. teleius and P. nausithous occur in wet grasslands, P. arion and P. rebeli inhabit dry grasslands, and P. alcon lives on moist heaths and bogs. In such biotopes, Phengaris butterflies live typically in closed populations with very little dispersal. All species are univoltine and are adult for approximately three or four weeks, with the time on wing varying by region and year, generally within mid-June to the first week of September. Individual butterflies have a very short life span, no more than one week, and they do not emerge all at once. Females deposit their eggs on specific host plants that flower in mid-summer. The host plants differ between species: P. teleius and P. nausithous use exclusively Sanguisorba officinalis [29], P. arion uses Thymus particularly T. polytrichus and Origanum vulgare and P. alcon, and P. rebeli uses Gentiana pneumonanthe. Their life cycle begins in mid-June with eclosion of the imagos. After mating, females start laying eggs in host plants, usually near the flower buds. At about three weeks after oviposition, depending on the weather, young larvae hatch and feed on the reproductive tissues of flowers of the host plant. At the end of the third instar, larvae leave the plant by letting themselves drop to the ground and then wait to be discovered. Foraging worker ants of particular species mistake them for their own brood, due to chemical mimicry, and carry them to their nests. The host ants are of the genus Myrmica Latreille, 1804 (Hymenoptera: Formicidae). Inside the ant nests, larvae are cared for and gain about 98% of their final biomass, before they pupate and leave the ant nest as adult butterflies after 10-11 months [30-31]. Some larvae can live for an additional year in the ant nests, for a total of about 22-23 months [32-33]. Larval survival is, therefore, dependent on the presence of two resources, and site selection for egg deposition by the females may be affected by either of them: (i) the specific food plant used as host for the phytophagous phase and (ii) a particular species of Myrmica used to complete the development inside the nests [34-37]. Obviously, the larvae will die if they cannot reach the flower reproductive tissues of the host plant, or if they subsequent fail to be adopted by ants [33]. Consequently, the relations between the butterfly, host plants, and ant colonies, are very complex and can differ between Phengaris species. The adoption process is very complex and is the goal of many scientific studies. The first challenge for success starts at the beginning of life cycle, with the right selection of suitable host plants for egg deposition. In recent years, several authors have studied the egg-laying preference of Phengaris butterflies. One of the most important factors influencing egg deposition is the distance between the larval host plant and the host ant nest [36, 38]. Patricelli et al [39] showed that P. arion select the plants for oviposition on the basis of bud phenology as well as the presence of host ants in the vicinity. Other results support an oviposition strategy based on host plant characteristics but offer no evidence for host-ant-based oviposition in P. alcon [30, 40]. After this phytophagous phase, the next challenge is the adoption of larvae by specific host ants. As social parasites of ants, Phengaris species possess myrmecophilous adaptations that enable them to interact and coexist with various Myrmica species [41]. These adaptations vary greatly among species according to the type of interaction, which ranges from invasion to full social integration [42]. Among the European Phengaris, this dichotomy is illustrated. Thus, the caterpillars of P. alcon and P. rebeli are cuckoo-
feeders, described as full integration inside the ant nests by processes of mimicry. Within this group, the caterpillars are able to mimic the ant larvae and therefore be fed directly, often by trophallaxis of nurse ants in the brood chambers [33]. By contrast, larvae of P. arion and P. teleius prey on the ant brood as “predatory species” [43]. No precise information on the feeding behaviour of P. nausithous is available, although according to Thomas and Settele [44], they may have an intermediate strategy. The cuckoo feeding strategy results in higher survival of the social parasites and a more efficient exploitation of the resource, when compared to the predatory species. Up to 67 times more imagos are produced per ant nest by cuckoo feeders’ than by those with a predatory strategy [45]. In the view of other authors, the act of colony penetration is frequently cited as the key challenge in the life of a social parasite [42]. Early studies on the host ants suggested that the success of Phengaris was due to each Large Blue species using a single Myrmica ant species (primary host) to complete its development [46]. They were only occasionally found inside other Myrmica nests (secondary host). The term “secondary” implies that colony penetration is rare, and that survival of the larvae in secondary host colonies is so low that the population is unable to persist on these alone [Thomas et al, 2005, cit by, 47]. Accordingly, the most predictable groups for Phengaris-ant hosts were: P. arion - M. sabuteli, P. nausithous - M. rubra, P. teleius - M. scabrinodis, P. alcon - M. ruginodis and M. scabrinodis and P. rebeli - Myrmica schencki. However, recent and repeated studies have demonstrated the multi-species use of host ants [28, 48-51]. For example, P. nausithous almost exclusively exploits Myrmica rubra nests in Europe, although M. scabrinodis is its host ant in a very isolated population in Transylvania (Romania) [52]. Also, P. arion was found in nests of three different ant species while its ‘primary host’ M. sabuteli was present but not infested by the larvae [51]. Many other studies have demonstrated the variation between regions and habitats of ant species used as larval hosts of Phengaris. Clearly, a complex ecological trilogy must occur for the survival of the most threatened butterflies in Europe.
Causes for decline and conservation approaches Many species are affected by anthropogenic and climatic events, but one or more processes are clearly changing in a major way in some Phengaris species, due primarily to the complexity of their lives, as explained above. Some meta-populations have been reduced to corpopulations and some of those have later disappeared [11]. This phenomenon is most visible in western Europe, where increases in industrialization and human population density have lead to the intensification of agriculture on the landscape or, by contrast, its abandonment. In the last decades of the 20th century, this landscape was severely changed: converted, abandoned or transformed into intensive grasslands with high inputs of fertilizers, or selective herbicides, together with modified mowing and grazing regimes. This led to the loss of many plant species, to profound changes in the vegetation, and in soil structure, with a subsequent disappearance of many Phengaris populations. The abandonment of patches by farmers led to an increase in vegetation height, and cover, and a subsequent loss of microclimates suitable for ants, whose nests support the final period of the Large Blue butterflies. These changes have a direct effect on the success of the species involved. During the flight period of the butterflies, any mowing compromises the deposition of eggs. The surviving females are unable to deposit eggs if host plants are not there. During this period, grazing also has a
very negative effect on populations because the eggs and the small caterpillars are eaten, and population success is compromised [53]. Nowadays, almost all the Phengaris populations live in small and isolated habitat patches. This isolation is worsened by the low inter-site mobility that is intrinsic to the genus, leading to minimal chances of exchange with other habitat patches, and thus reduced viability of future populations. Recent research has led to the development of meta-population models, showing that the probability of local extinction in a patch is assumed to be proportional to its area, whilst the probability of colonization of an empty patch is determined by the distance from occupied patches and their area [54-55]. The quality of a suitable Phengaris site can influence the local butterfly population size and perhaps also persistence [56]. Multiple factors contribute to habitat quality and management practices need to take this in account. In the case of threatened species, conservation managers should anticipate the species requirements at different spatial levels, ranging from habit quality to habitat network design at a global level [57]. Accordingly, conservation efforts should not only be limited to the specific habitat of target species but should also be expanded to sites with potential for that species success. A good example of the application of conservation measures occurs with the Large Blue species, P. arion. Following its extirpation from the UK in the 1970s, caused by cessation of sheep grazing, this species has been subject of very intensive conservation measures. Much work was done on habitat restoration, to allow the reintroduction of the species in Britain with remarkable success. According to Mouquet et al. [58], P. arion can be safeguarded only by preserving traditional management practices. Another success for European insect conservation was the reintroduction of two Large Blue butterfly species, P. teleius and P. nausithous, in the Netherlands in 1990. Until the 1970s, both species had occurred in the centre and south of the country but, due to agriculture intensification, had then disappeared from the country. Ten years after reintroduction into the Moerputten nature reserve in the southern province of NoordBrabant [11], the populations developed well and increased in numbers [59]. Although these species have very similar life histories, they require different approaches to their conservation due to subtle differences in adult habitat use and movement. While the conservation of P. teleius should concentrate on improving local habitat quality, the conservation of P. nausithous is predicted to be more effective by creating a spatial network of suitable habitat plots, such as along road verges. In general, several conservation strategies have been used to preserve and increase populations of Phengaris species. Mowing and grazing are the most discussed management measures; either because they influence the abundance of plants, or that of the specific ants that depend on the open conditions created by these practices. Wynhoff et al. [60] state that the mowing of butterfly habitat should be avoided between midJune and mid-September, as this would remove the flower heads on which the butterflies lay the eggs. Also, one of the main goals of mowing should be the increase of nest densities of Myrmica species by creating open vegetation and a warm climate at soil level. However, it is also essential that the recommended mowing regimes are relevant to the Myrmica species being protected, because there are different ecological exigencies within species. For example, while the sites of M. rubra should be left undisturbed until the end of summer and mowing should be made in late autumn, the promotion of M. scabrinodis can occur with any mowing happening early in the year.
Conclusion Unlike the anthropocentric management of the past, the present land managers in Europe are worried about the loss of biodiversity. So as to raise awareness, major attention has been given for a long time to charismatic groups of flora, of wildlife, and later to a genus of insects such as these in the Lepidoptera. From a holistic point of view, all the organisms are important and “wildlife-friendly” management is therefore advocated. For successful conservation of natural habitats for endangered and threatened species, monitoring studies are required and specific policies need to be undertaken in both longand short-terms. For the Phengaris group, the key processes affecting the species viability and the habitat-types that are at risk were identified here. A complex ecological trilogy involves the species, particular vegetation types in their habitat, and a specific ant host. Useful management practices were discussed. For the survival of the most threatened butterflies in Europe, it is obviously necessary to directly involve local communities in order that they recognise what is special about Phengaris butterflies and their conservation needs. Not only the increasing of the existing Phengaris populations but also the creation of new suitable sites should be of concern. We propose for the shortterm, in order to successfully achieve this goal, extension work with people to promote adequate management procedures whenever necessary, monitoring of the specific habitats, and an expansion of monitoring to sites with future potential for the endangered species.
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