The saproxylic beetle, Cucujus cinnaberinus, has received increasing research attention in Europe since the adoption of the Habitats Directive and establishment of the Natura 2000 network. The history of the species has been investigated as well as the influence of abiotic and biotic variables on the distribution of C. cinnaberinus in Slovenia which is at the limit of its range and also terra typica for the species. The species was first described in 1763 by Joannes A. Scopoli in Carniola, a duchy of the Habsburg Monarchy. Today, most of the territory of Carniola is situated within Slovenia. C. cinnaberinus is particularly common in the eastern part of the country, but very scarce in the mountainous western part. According to historical and recent distribution patterns of C. cinnaberinus in the former Carniolan territory, the region of Ribnica-Kočevje in southern Slovenia is proposed as the most probable type locality of the species. Although the bulk of the C. cinnaberinus population in Slovenia is confined to the lowlands, the species has been found up to 1095 m a.s.l., albeit at a much lower abundance due to the influence of climate and forest structure. Although C. cinnaberinus is a quite an opportunistic species regarding host tree selection, it has been shown to exhibit a preference for Tilia, Populus and Robinia. It is suspected that the high abundance of C. cinnaberinus in lowland floodplain forests is due to the recent human-induced increase in preferred fast-growing and short-lived host trees, i.e. the planting of poplar trees and spread of invasive Black Locust (Robinia pseudoacacia) after the 1960s. In contrast, in montane forests, preferred host trees (e.g. Tilia) represent < 1 % of all growing stock. Although montane C. cinnaberinus populations are rare, they could still be important for the conservation of the species, since montane habitats cover the largest area within the species’ distribution range.

saproxylic beetle, Natura 2000, type locality, Carniola, altitudinal distribution, host tree selection, macrohabitat, large-scale survey

The Directive on the Conservation of Natural Habitats and of Wild Fauna and Flora or the Habitats Directive (92/43/EEC) was adopted in 1992 and subsequently spurred intensive research activity on species of conservation concern in Europe. This is particularly evident with respect to the saproxylic beetles which is amongst the most threatened beetle groups in Europe (Nieto and Alexander 2010) and is reflected in the number of published papers listed in the Web of Science on 21 saproxylic beetle species of conservation concern, with 87 % of all papers published after the year 1992 and, in particular after 2010, when more than 50 % of all papers were published. However, research activity has been skewed towards more widespread and charismatic species (e.g. Ranius et al. 2005, Harvey et al. 2011), at least that concerning species ecology, monitoring, distribution and conservation biology (see Appendix 1: Table S1).

There are only four well studied species in this sense, namely Osmoderma eremita, Morimus funereus, Lucanus cervus and Rosalia alpina and three moderately studied species (Cucujus cinnaberinus, Cerambyx cerdo, Limoniscus violaceus), while the majority of species have been poorly studied or not studied at all. While this deficiency in research greatly hampers the conservation management of Natura 2000 sites, on the other hand, it stimulates applied research on species survey methods, monitoring and conservation management (e.g. Bussler and Müller 2009, Carpaneto et al. 2010, Harvey et al. 2011, Bergman et al. 2012, Gouix and Brustel 2012, Chiari et al. 2013, Walentowski et al. 2013, Gough et al. 2014, Le Gouar et al. 2015, Campanaro et al. 2016, Carlsson et al. 2016, Hopkins and Thacker 2016, Larsson 2016).

Until recently, Cucujus cinnaberinus was considered as a poorly known species (Horák 2011). It is confined to Europe and is distributed from the Mediterranean to Scandinavia and from Russia to Spain, but with a scattered distribution pattern, probably due to past population decline and local extinctions (Horák and Chobot 2009, Horák et al. 2010). The species has however an extremely cryptic lifestyle, as the larvae and adults live under the bark of dead tree trunks (Horák et al. 2008) and this might also be a reason for the low detection rate of the species in the past (Horák et al. 2010).

Recently, field survey techniques have shifted from focusing on adult beetles to the detection of larvae under the bark which appears to be a much more efficient detection method (Bussler 2002, Straka 2006, Vavra and Drozd 2006, Horák and Chobot 2011, Vrezec et al. 2012, Gutowski et al. 2014). By applying the larval survey technique, new discoveries of the species have accelerated, as have rediscoveries in regions where the species was previously thought to be extinct (Mazzei et al. 2011, Kovács et al. 2012, Fuchs et al. 2014, Holly 2014, Mainda 2014, Hörren and Tolkiehn 2016, Šag et al. 2016, Tovar and Baena 2016). This intensified research activity uncovered new records of other Cucujus species and led to the discovery of a new endemic species in Europe (Horák et al. 2009, 2011, Bonacci et al. 2012, Gutowski et al. 2014). Horák et al. (2008, 2010) claimed that the C. cinnaberinus population stronghold is situated in central European countries, although this might change due to increasing knowledge on species distribution and abundance in southern Europe (Mazzei et al. 2011, Vrezec et al. 2011, Kovács et al. 2012, Šag et al. 2016).

In 1763, Joannes A. Scopoli described the species as Meloe Cinnaberinus from Carniola (also Carniolia, Krain, Kranjska), a duchy of the Habsburg Monarchy. Today, most of the Carniolan territory is situated within Slovenia (Figure 1), where the type specimen originated (Scopoli 1763). This fact has however been largely neglected in recent papers (e.g. Horák and Chobot 2009, Horák et al. 2010, Bonacci et al. 2012) partly as a result of the lack of knowledge about the type locality of C. cinnaberinus (i.e. the Duchy Carniola was frequently misinterpreted in the past; Baker 1999) which was not specifically mentioned in the original description of Scopoli (1763) and partly as a result of lack of knowledge on the recent status of C. cinnaberinus in the former Carniolan territory and the current Slovenian territory (Pirnat and Drovenik 2004, Horák et al. 2010, Vrezec et al. 2011). Therefore, the aim of this paper was to review historical and recent knowledge about the distribution of C. cinnaberinus in its terra typica in Slovenia, with special emphasis on J. A. Scopoli’s research activity in the region (Petkovšek 1977, Baker 1999, Štih et al. 2008), in order to identify the most probable type locality of the species. As C. cinnaberinus is highly genetically polymorphic (Røed et al. 2014), it is essential to define the type locality as a population reference for further taxonomic and phylogenetic studies of this and related species.

Taking into account recent distribution maps of C. cinnaberinus (Horák et al. 2008, Horák and Chobot 2009), it seems that Slovenia represents the limit of the species’ distribution since there is no population known in the western neighbourhood of Northern Italy (Brandmayr et al. 2016). This situation presents the opportunity to study the species’ micro- and macrohabitat selection patterns at the edge of its distribution, where it is rarer and less abundant. So far, the species’ habitat parameter associations have been intensively studied only in central Europe, in its population stronghold where it is very abundant and its population is even expanding (Horák et al. 2010, 2011). This study therefore aimed: (1) to assess horizontal and vertical distribution patterns of C. cinnaberinus in Slovenia at its distribution edge, based on large-scale field sampling guided by a potential distribution model; (2) to review historical data of species occurrence in Slovenia from 1763 onwards and (3) to determine species macro- and microhabitat selection patterns to assess the limitation parameters of the species’ distribution at the edge of its range.

Figure 1.

The Duchy of Carniola (dark grey) in the period of Joannes A. Scopoli’s research activity between 1754 and 1769 with Carniolan provinces marked with their original Latin names. Recent state borders in the region are marked in the background. The map was redrawn after Florjančič de Grienfeld (1744).

This study revealed that, within the former Duchy of Carniola, where C. cinnaberinus was described for the first time (Scopoli 1763), there are at least four regions that may represent the species’ type locality. It is known however that J. A. Scopoli obtained zoological and botanical material for his studies from only two of these regions (Petkovšek 1977, Baker 1999): the Branica River Valley near Vipava and the montane forests of the Ribnica-Kočevje region. The review of C. cinnaberinus records showed that the beetle was present in moderate abundance only in the Ribnica-Kočevje region in the past and recent records show a similar pattern. It is known that J. A. Scopoli himself visited the region around Ribnica several times, especially in the autumn when he collected mushrooms (Petkovšek 1977). Additionally, he obtained material, predominantly plants, from the vicinity of Kočevje from a colleague Franz Xaver von Wulfen (Scopoli 1772, Petkovšek 1977). In his description of C. cinnaberinus, Scopoli (1763) noted “Octobri M. in Brassica oleracea capitata repertus & adlatus”, meaning that “The species was found on a cabbage head and brought to him in mid October”. Since C. cinnaberinus is a strict saproxylic species living under the bark of dead trees and with a limited flight season in spring and also in autumn (Horák and Chobot 2011), it is argued that the discovery of the specimen on a cabbage plant suggests only an occasional finding of a single specimen. It is very unlikely that such a finding would be recorded where the species is extremely rare such as in the Branica River Valley where only one record exists from 2002 and where the species was not confirmed again in later intensive surveys. The area is apparently the westernmost limit of the species distribution in SE Europe since there is no record known for the species further to the west in northern Italy (Horák and Chobot 2009, Brandmayr et al. 2016). Conversely, in the Ribnica-Kočevje region, C. cinnaberinus was reported in historical surveys (in 1930s and 1970s) as well as in recent surveys after 2008 at a moderate trunk occupancy rate of 10 %. Therefore, it is proposed that the Ribnica-Kočevje region in southern Slovenia with Mts. Velika gora, Stojna, Kočevski Rog and Stružnica are the most probable type locality for C. cinnaberinus. Despite intensive field studies, no other Cucujus species has been recorded in Slovenia neither recently nor in the past and this may decrease the possibility of misinterpretation of Scopoli’s specimen as an identity of C. cinnaberinus.

Throughout the 19^th and 20^th century, C. cinnaberinus was considered as an extremely rare species in Slovenia with few known records and a similar pattern was suspected in other parts of Europe (see literature review in Horák et al. 2010). However, even large populations could have gone undetected due to the species’ elusive behaviour and sparse distribution or due to ineffective survey procedures (McDonald 2004). The latter was particularly evident in C. cinnaberinus, with a dramatic recent increase in records after application of the larval search method and the pattern over the last century is remarkably similar in Slovenia as well as in other countries (Horák et al. 2010, Eckelt et al. 2014). Moreover, this type of data increase is expected in most of the beetle species listed in the Habitats Directive due to an increase in research after the Directive’s adoption (see Introduction for literature review). The results from this study and reports of new discoveries of C. cinnaberinus populations in many countries across Europe (see Introduction for literature review) are not in accordance with the interpretation of Horák et al. (2010) that rarity and species absence, especially in southern European countries, is a result of population extinctions or decline in the past, but rather it is a consequence of research deficiency and overlooked populations. A Europe-wide study evaluating the population status of C. cinnaberinus and taking into account abundance estimates and research efforts to reveal species distribution and its population strongholds is thus needed. It was confirmed that the observations of Horák et al. (2010) about species population strongholds being limited to lignicultures and riparian forest stands including stands of fast growing invasive alien trees such as Black Locust (Robinia pseudoacacia) also hold true in southern Europe. Surprisingly, there were no historical records for C. cinnaberinus known from these sites in Slovenia which might support the hypothesis that the recent population expansion is due to a change in the structure of riparian forests due to intensifying poplar lignicultures and spread of invasive non-native tree species (Horák et al. 2010, Eckelt et al. 2014, Fuchs et al. 2014, Hörren and Tolkiehn 2016). In Slovenia, this was particularly true in lowland floodplain forests, in which there was intensive poplar planting in the period from 1960–1980 (Božič and Krajnc 2012) and rapid expansion of the Black Locust which regionally had already reached more than 6 % of the growing stock in the forests (Kutnar and Kobler 2013). Nevertheless, C. cinnaberinus was found in a wide altitudinal range from the lowlands up to 1095 m a.s.l. in Slovenia, up to 1400 m a.s.l. in Austria (Eckelt et al. 2014) and even above 1500 m a.s.l. in Albania (Kovács et al. 2012). The field study based, on a preliminary species distribution model, revealed that higher elevation montane forest stands could represent a significant part of the species’ distribution range by surface area, although, in these habitats, the species was much less abundant than in the lignicultures and riparian forests of the lowlands.

Due to low abundance, there have been few studies actually reporting the species from montane habitats (e.g. Holzer and Friess 2001, Bussler 2002, Mazzei et al. 2011, Kovács et al. 2012, Eckelt et al. 2014) and, therefore, a major part of the species’ distribution range has not been considered in conservation plans. More studies and conservation efforts for C. cinnaberinus are thus needed in montane and traditional forest habitats. Focusing only on current population strongholds found in poplar lignicultures and even in invasive tree species stands in the lowlands might be a Trojan horse in C. cinnaberinus conservation efforts (Horák et al. 2010). The development of more efficient detection methods based on species pheromones or other semiochemicals that attract species would be helpful in further conservation studies (Larsson 2016), especially in sub-optimal but widespread species habitats.

In this study, low as well as high elevation habitats were included and, in both habitats, the amount of deadwood, amount of deciduous trees and degree of canopy openness was positively associated with C. cinnaberinus probability of occurrence, a fact which was in agreement with other studies on species habitat preference (Horák et al. 2010, Horák et al. 2011). Altitude had a negative effect on species distribution, meaning that, in stands with the same amount of deadwood, the species would be less abundant at higher elevations. A possible explanation could simply be macrophysiological. In ectotherm species, a restricted optimal temperature window at higher altitudes in comparison with lower altitudes might play a decisive role in the species’ overall metabolic performance which is reflected in its life-history traits, including its reproduction and development rate (Gaston et al. 2009). Although the development cycle is still not well studied in C. cinnaberinus, Palm (1951) reported that larval development should take at least two years. Nevertheless, the duration of larval development could differ greatly between different climates, as shown for example in the stag beetle (Lucanus cervus), in which the duration of the larval stage can vary from 3 to 6 years and even the number of larval instars can differ regionally (Harvey et al. 2011). C. cinnaberinus is a widespread species, ranging from boreal to warm temperate climates (Horák and Chobot 2009) and also has a wide altitudinal distribution as shown in this study. Its metabolic performance and life history traits might however change with latitude and altitude. Overall, it seems that the species’ optimal conditions are in middle European lowlands in a warm temperate climate with hot and humid summers (Kottek et al. 2006, Horák et al. 2010). In Slovenia, such conditions are found only in the eastern part of the country, while the rest of the country is mountainous, which might be the reason for the lower C. cinnaberinus abundance. A second explanation for the effect of altitude could however be ecological, i.e. differences in habitat quality in lowland vs. montane forests. In future studies, the effects of climate conditions on C. cinnaberinus distribution patterns should be further examined, especially the effects of temperature and precipitation, to reveal their direct impacts on species life cycles and possible indirect impacts due to habitat structure alterations.

The size of the deadwood has been shown in this and other studies to be important for saproxylic beetles which prefer longer tree trunks with a larger diameter (Jonsson et al. 2005, Lindhe et al. 2005, Jonsell et al. 2007, Jonsell 2008). Although C. cinnaberinus was found in a number of host tree species and tree species was not found to be an important predictor in species microhabitat selection in lowland forests (Horák et al. 2011), it was found that tree host species might be important in the overall microhabitat performance of C. cinnaberinus. In such opportunistic species, the availability of host tree species should play a crucial role in host selection, where the most abundant tree species in a particular forest stand is also the most frequently occupied. That was the case for Salix in our sample of inspected trees and for Pinus in Southern Italy (Mazzei et al. 2011).

On the other hand, preferred or optimal tree hosts that are selected in a larger proportion than that available, could facilitate species establishment, population growth or even spread. Tilia, Populus and Robinia in particular, as tree species, were significantly preferred by C. cinnaberinus. Various poplar species were frequently reported as host trees of C. cinnaberinus in lowlands as well as in higher elevation forests (Horák et al. 2010, Eckelt et al. 2014, Marczak 2016). In this study, in addition to poplars, invasive Black Locust was found to be the preferred tree host in lowland forest. In addition to Robinia, other alien tree species, such as Aesculus and Ailanthus, were also reported as host trees in Austria, although at low frequencies (Eckelt et al. 2014).

The significant shift from native to invasive tree hosts revealed in this study indicates the great adaptive potential of C. cinnaberinus, particularly for rapid growing and short-lived species which could produce larger quantities of deadwood mass over shorter periods. The increase in growing stock and consequently in the deadwood of preferred host tree species in lowland forest stands in Slovenia, especially of Populus and Robinia, started in the period from the 1960s onwards (Božič and Krajnc 2012, Kutnar and Kobler 2013) and probably created optimal habitat conditions for C. cinnaberinus, resulting in an increase in its population and its eventual spread (Horák et al. 2010).

In contrast, there are no such conditions in montane forests where trees such as Fagus, Abies and Picea predominate in the growing stock (Marinček 1987) but were not found amongst the preferred species in this study or in those of others (Eckelt et al. 2014, Marczak 2016). On the other hand, Tilia, which is a preferred host tree in montane forests, has a low growing stock (<1 %) in the montane forests of Slovenia (Puncer 1980) and, therefore, the abundance and population size of C. cinnaberinus is constrained in these stands. Montane C. cinnaberinus populations thus remain low and scattered despite the beetle also being found in other dominant tree species in these environments, including Fagus, Abies and Picea (Eckelt et al. 2014, this study).

In conclusion, this study presents new findings regarding the ecology of C. cinnaberinus at the limit of its distribution in two types of species habitat that greatly differ in species abundance and overall ecological performance: lowland and montane forests. The study revealed the importance of montane forests for C. cinnaberinus conservation, although recent population strongholds are located in lowland riparian forests and lignicultures, these being a consequence of human-induced changes in forest structure due to poplar plantings and expansion of fast growing alien tree species.

To evaluate the future potential of C. cinnaberinus expansion and to define conservation management of existing populations, it is necessary to explore the impact of environmental factors that limit the species’ distribution, in particular climate (effects of environmental temperature and precipitation) and tree species structure in forest stands. Future environmental change scenarios (climate change, invasion of alien tree species) may cause C. cinnaberinus population decline in some regions as well as an increase and expansion in other regions of Europe due to the apparently high dispersal and colonisation capacity of the species (Horák et al. 2010).

Field surveys and research work were funded by several projects during the period 2008–2017: Monitoring Programme of Natura 2000 beetle species in Slovenia (funded by the Ministry of the Environment and Spatial Planning), CRP project “Indicators of conservation status and measures for sustaining favourable conservation statuses of species and habitat types in the Natura 2000 forestlands–V4-1143” (funded by the Slovenian Research Agency and Ministry of Agriculture, Forestry and Food), Life+ project LIVEDRAVA (LIFE11 NAT/SI/882; lead partner DOPPS-BirdLife Slovenia), GoForMura (funded by EEA and Norway grants) and research core funding No. P1- 0255 (funded by the Slovenian Research Agency). Philip Jan Nagel made linguistic corrections for the paper.

Special issue published with the contribution of the LIFE financial instrument of the European Union.