New mesocarnivore at the doorstep of Central Europe: historic development of golden jackal (Canis aureus) population in Slovenia

Golden jackal (Canis aureus) has dramatically increased its distribution and abundance in Europe. Expansion is now reaching parts of Central, Northern, and Western Europe, where jackal occurrences are mainly limited to vagrants or single territorial groups. Currently, it is hard to predict future development of jackal populations in these regions, as it remains unclear whether environmental conditions here could enable population growth similar to the jackal core areas in the South-eastern Europe. We used a combination of a literature review, opportunistically collected data and systematic acoustic surveys to study historic development of golden jackal population in Slovenia, a Central European country that jackals started colonizing 70 years ago and which could serve as a model for other countries at the expansion frontier due to its resemblance in environmental conditions. After the initial expansion waves reached Slovenia in the 1950s and 1980s, jackal presence became more permanent since 2000s. This is also the period when first territorial groups and reproductions were confirmed, but it was not until the following decade for the number of records to start exhibiting an exponential growth. By 2016–2017, the minimum densities in lowlands reached 0.06–0.29 jackal territorial groups/10 km2, which is still lower compared to the core areas in the Balkans and the Pannonian Basin. This study demonstrates that jackals can successfully colonize and spread across a forested Central-European country with lower availability of anthropogenic food resources, although in such conditions, it can take several decades of sporadic existence before population progresses into exponential growth similar to jackal populations in the European core areas.


Introduction
Among all of the native carnivores of Europe, the golden jackal (Canis aureus) is currently exhibiting the most dramatic expansion (Trouwborst et al. 2015), but its basic ecology remains poorly studied (Krofel et al. 2022a). Jackals most likely colonized Europe during the Holocene, but were then for millennia limited to a few islands and coastal regions (Krofel et al. 2017). First increases in their distribution range were observed during the nineteenth century, while a rapid expansion started after the Second World War and continues nowadays. Recent research suggests that the most likely trigger of this expansion was continental-wide persecution of the European apex predator, the grey wolf (Canis lupus) (Krofel et al. 2017;Newsome et al. 2017). After or in parallel with the mesopredator release, also other factors could have eased the jackal expansion, including climate change (Fabbri et al. 2014), anthropogenic food sources (Krofel et al. 2017), the Balkan wars (Tóth et al. Communicated by Rafał Kowalczyk. 1 3 2009), as well as changes in the land-use (Šálek et al. 2014) and/or hunting management (Markov 2012).
Increase of jackal abundance was especially notable in the South-eastern Europe with exponential growth reported from many areas in the Balkans and Pannonian Basin. For example, the jackal distribution range in Bulgaria increased 33-fold between 196233-fold between and 198533-fold between (Kryštufek et al. 1997, in Serbia and Hungary hunting bag statistics suggest an exponential population growth since the 1980s (Heltai et al. 2013), and in Bosnia and Herzegovina an average 35% annual increase in hunting records had been reported since 2000 (Trbojević et al. 2018).
In contrast, jackals started occurring in most parts of the Central Europe only in recent decades and have been so far exhibiting much slower population growths (e.g., in Slovakia; Guimarães et al. 2019), while in many countries, such as Germany, Switzerland and Poland, jackal occurrences are still mainly limited to vagrant animals or single territorial groups (Jirku et al. 2018;Kowalczyk et al. 2020;Tillmann 2020). At the moment, it is hard to predict future development of jackal populations in most of the Central, Northern and Western Europe. Two mutually non-exclusive hypotheses could explain slower expansion and current lower jackal abundances in this part of the continent: 1) longer distance to the origin, and 2) different environmental conditions. According to the 'distance' hypothesis, the main expansion wave has not yet reached northern and western parts of Europe, but once it will, similar densities to those currently in the South-eastern Europe could be expected. 'Environmental' hypothesis on the other hand suggests that different (abiotic and biotic) environmental conditions, such as climate, competitors and food availability, are less suitable outside of the current core areas and jackal abundance in these regions will never reach those reported from the Balkans and Pannonian Basin. Resolving this question could help to predict future development of European jackal populations outside of the current core area in the South-eastern Europe.
Here we review historic development of golden jackal population in Slovenia, which could serve as model for the other Central and Western European countries, due to its resemblance in environmental conditions, as well as human densities, land use, hunting and waste management. However, jackals have first arrived to Slovenia already more than 70 years ago, thus it provides a unique example of a long-term development of a jackal population in a Central-European setting. This is the first attempt to gather available data on jackal occurrences in Slovenia during almost seven decades of its population development. We 1) conducted a systematic literature review, including collection of notes from the grey literature and hunting magazines, 2) gathered available non-published mortality, sighting and camera-trap records, and 3) conducted the first systematic howling surveys of territorial jackal groups in parts of Slovenia with reported or assumed jackal presence, including repeated surveys in some areas to determine abundance trends in time.

Study area
The study was carried out in Slovenia (total surface area: 20,271 km 2 ), a Central European country neighbouring the Balkan peninsula, where four biogeographic regions meet: the Pannonian, the Alpine, the Dinaric and the Mediterranean. The topography and climate are reflecting the regional differences with a range of altitudes (averaging at 557 m, range 0-2864 m) and climate types (continental, subalpine, alpine and sub-Mediterranean) across the country. The average annual temperature is 8-10 °C (with 0 °C in the mountainous areas and 12 °C at the coast) and average annual precipitation is between 1100 and 1200 mm (with 900 mm in Pannonia and 3200 mm in the Alps). Snow cover lasts from 50 days at lower altitudes and up to several months at higher elevations. The vegetative growth period lasts from March to November in lowlands, with delays in higher regions. The habitat is heterogeneous, including forested hilly landscapes, dry grasslands, high montane areas, wetlands, as well as human-dominated agriculture land and urban areas. Average human density is 104 inhabitants/km 2 with majority of larger settlements concentrated in the lowlands (Slovenian Statistical Office 2023).
The four study areas where repeated acoustic surveys for golden jackal were performed include Ljubljansko barje, Zgornje Posočje, Kras and Bela Krajina (Fig. 4). Ljubljansko barje is a lowland marshland (average altitude is 297 m) in the centre of the country, characterized by regular flooding, extensive grasslands, peatland and bogs. Most of it is agricultural land with draining canals. Zgornje Posočje is the upper valley of the Soča river, lying amidst the Julian Alps and being highly influenced by the Adriatic, bringing high precipitation (an average of 2900 mm). It is mainly covered by cultivated land and settlements in the valleys and forested slopes dominated by common beech (Fagus sylvatica) and high Alpine peaks above it. Kras is a low karstic plateau (with an average of 470 m altitude) in the South-western part of the country with characteristic karstic geology, having almost no surface water and low forest cover (up to 30%). More than half of the plateau are dry grasslands and pastures, interrupted by forest patches and shrublands. Bela Krajina is located in the South-eastern part of Slovenia and is framed by river Kolpa in the South-East and Dinaric mountains in the North-West. It is characterized by a mosaic of lowland forest of sessile oak (Quercus petraea) and European hornbeam (Carpinus betulus), meadows and pastures.
In all four areas, roe deer (Capreolus capreolus), red deer (Cervus elaphus) and wild boar (Sus scrofa) are regularly present and in Zgornje Posočje also Alpine chamois (Rupicapra rupicapra) can be found. Wolves are occasionally present in all areas, while the core area of wolf population with permanent packs is located in the neighbouring Dinaric mountains (Ražen et al. 2020).

Literature review
We conducted a systematic literature review with the use of online search engine (GoogleScholar) and manual review of the notes from the hunting magazines, available grey literature, and all Slovenian journals publishing results of archaeological and paleontological excavations. We augmented our literature search using snowball sampling (searching the references of papers we reviewed).

Opportunistic data collection
We started collecting opportunistic data in the 1980s and conducted interviews with hunting club members on occurrence of jackals since 1998. Collection of opportunistic data became more systematic after 2005, when we re-established a network of people (hunters, foresters, wildlife managers, rangers from protected areas, zoologists and other local nature enthusiasts) from the entire country to ask for opportunistic records of golden jackals. We personally interviewed them over phone and appealed to them to inform us with any information about the future records of golden jackals in their areas. We did not increase our efforts to reach a wider pool of people over the study period so we assume the effort to collect opportunistic data over the years remained relatively constant until 2018, when collection of opportunistic data discontinued.
We categorized the opportunistic data into three categories: mortality (legally shot, illegally shot, roadkill), spontaneous howling (including responses recorded during the wolf howling surveys; Ražen et al. 2020) and other reliable records (direct observations, photo or video material from personal cameras or camera traps, photos of tracks and faeces). The data that we could not verify was not included in the database, e.g., 13 cases of illegally shot animals were reported without any proof (photos or carcasses) and were omitted from the analysis. Each opportunistic record was collected with its spatial and temporal attributes, i.e., the date (if exact date was not available, at least the year of observation was noted), the GPS coordinates (in some cases assigned later, based on the description of the location), and other observation details, including the name of the observer and potential records of reproduction (e.g., gravid female or presence of pups).

Acoustic surveys
An acoustic (play-back) method was used to determine the presence of territorial groups of jackals, following the study design developed previously in other parts of Europe (e.g., Giannatos et al. 2005;Krofel 2008;Šálek et al. 2014). Acoustic surveys focused on four study areas, where highest number of opportunistic records were recorded: Ljubljansko barje (no. of calling stations: 12), Zgornje Posočje (32), Kras (22) and Bela Krajina (30) (Fig. 4). Each of these areas was divided into 4 × 4 km grid and within each cell one or more calling stations were selected from which a recorded group yip-howl by three to four jackals was broadcasted. Calling stations were selected according to topographical characteristics in order to optimize sound transmission. We avoided sources of background noise (main roads, settlements). Field work was not done on windy or rainy nights.
Each broadcasted howl lasted for 30 s and was followed by a 5-min pause. If there was no response, this set of broadcast and pause was repeated four to five times on each calling station, which totalled to five to six broadcasts and overall session time of approximately 25-30 min. When jackals responded to the broadcast, we determined the direction of howling jackals using a compass. In order to avoid doubling we marked each response direction topographical maps. Geographical coordinates and altitude of locations were recorded by GPS (Garmin eTrex Summit). We also noted the time needed for jackals to respond and the number of howling jackals (single or a group). At calling stations located in open habitats we also tried to make a direct observation of jackals using night vision goggles (Dipol D212 PRO). After response we also scanned the area with a spotlight (2 000 000 cd light power). We always began with the survey at least one hour after sunset and finish at least one hour before sunrise.
For the calculation of minimum average jackal density estimates in four areas with repeated surveys, we followed approach used in previous studies (e.g., Giannatos et al. 2005;Banea et al. 2012;Šálek et al. 2014;Trbojević et al. 2018) to enable comparison with other parts of Europe. Human hearing distance of jackal howling on windless nights with no background noise was estimated to be 1.8-2 km (Giannatos et al. 2005), which results in an average effective area for an audible response from jackals to 10.2-12.6 km 2 . If the sound of transmission was hindered in one of the directions due to topographical features, we subtracted the corresponding share of the effective area, i.e., when we estimated that topographic obstacle hindered sound transmission to one of the cardinal directions, we subtracted one quarter of the area. Sound transmission was not hindered in more than one direction at any of the calling stations. It was assumed that only territorial groups of jackals were responding to the broadcasted howls and that each response direction coincided with a different territorial group. When several surveys were repeated in the same area, the most recent average value for annual minimum density per area was used in comparison with minimum jackal group density estimates from other European countries (Table 2).

Results
We collected data on the presence of golden jackals in Slovenia from the first detection of wild jackals in 1952-1953 until our last systematic survey in 2017. In total, during this period we collected 188 opportunistic records of jackal presence, including 75 records of direct observations, 55 records of mortality, 26 records of spontaneous howling (plus six records of jackal howling detected during wolf howling surveys), 25 photos or videos of jackals, and 2 records of indirect signs of presence (one scat and one footprint) (Figs. 1 and 2). Systematic monitoring of golden jackals in Slovenia with the use of acoustic surveys was initiated in 2006 in Central and South-western Slovenia. Since then, it was conducted every year except in 2008 and 2012, with considerable increase in effort since 2013, when we expanded surveys to the Pannonian lowlands, Julian Alps and Dinaric Mountains (Figs. 3 and 4). In total, 33 acoustic surveys have been performed with a total of 263 broadcasted playback series and 47 recorded responses from jackal territorial groups (Figs. 1 and 4). In four study areas we repeated surveys from 3 to 9-times, which enabled us to estimate relative trends in jackal densities in time (Fig. 5).
According to the literature review, the only potential (sub) fossil find of a golden jackal reported from Slovenia was a metacarpal bone from cave Babja jama near Ljubljana, but its determination was not clear and possibly belonged to a dog (Pohar 1985). Therefore, according to the fossil and historic records, golden jackal was most likely not present in Slovenia before twentieth century, similar to conclusions of earlier overviews for this part of Europe (Rakovec 1975;Sommer and Benecke 2005). First occurrence of golden jackal in Slovenia was reported in 1937 when a single animal, most likely from captive origin, was shot on Golovec near Ljubljana (Anonymous 1937). First wild animals were reported  (Mehora 1953;Brelih 1955). After this and until 1980, no further observations of golden jackals were reported. Between 1980 and 2000, rare but regular observations of vagrant individuals were recorded across Slovenia, but mostly limited to lowlands (Kryštufek and Tvrtković 1990;Kryštufek 1998). After 2000, reports of jackal sightings and other records become more frequent and widespread. In Eastern (Pannonian) Slovenia, the trend of spatial advancement of golden jackal was less pronounced as in the Central and Western part of the country. First territorial groups in Slovenia became established in the 2000s, with the first unconfirmed record of jackal territorial vocalization reported in South-western Slovenia in 2002 in Zazid, Kras (T. Mihelič, pers. comm.). The acoustic surveys were initiated in 2006, but acoustic responses were not detected in the first years of monitoring efforts. The first territorial group was confirmed with this method on Ljubljansko barje in 2009 (Krofel 2009). After 2010, there has been a steady increase in number of detected territorial groups of golden jackals from many parts of the country, but mostly in the lowlands (Fig. 2). In the Alpine region, jackals were detected since 2005, when one individual was accidentally shot in Kamnik-Savinja Alps (Krofel and Potočnik 2008). Since 2009 jackals have been regularly recorded in the Julian Alps, especially in Zgornje Posočje (Mihelič and Krofel 2012), where we confirmed first territorial group in 2013. In the Alpine area, jackals stayed mostly confined to valleys or foothills. Jackal records were less widespread also in Dinaric Mountains (South-Central Slovenia), where territorial groups are mostly limited to open habitats in anthropogenic areas outside core areas of wolf territories (Krofel et al. 2017 ; Fig. 4).
The highest density of jackal groups was estimated for Kras (Table 2), which is also the study area where we observed the fastest population growth in Slovenia, while in other three regions with repeated surveys the increase was more gradual (Fig. 5). On average, the jackal density estimates in Slovenia were in 2016 and 2017 still lower compared to the estimates reported from the South-eastern Europe (Table 2).
In total, we recorded 55 mortalities in 1953-2017 with numbers increasing considerably in the last years (Table 1). Most (65.5%) of the dead jackals were adults, while 7.3% were juveniles (three males and one female) and remaining were animals of unknown age. We were able to obtain information about the sex for 40 animals, among which males outnumbered females in a ratio of 1.9:1.

Discussion
Historic overview of golden jackal records in Slovenia showed that the species has been occurring in the country since the 1950s. Based on the data gathered, the development of the population in Slovenia can be divided into five distinctive periods with different dynamic of jackal occurrence: (1) absence of wild jackals (until 1952), (2) occasional occurrence of long-distance dispersers   (Figs. 1 and 2).
First golden jackals that appeared in Slovenia in 1950s were most likely long-distance dispersers from Dalmatia (Rutkowski et al. 2015). This period coincides with an expansion wave of jackals reported also from the Balkan peninsula and Pannonian basin, which brought the species for the first time to such high latitudes (Krystufek and Tvrtković 1990;Tóth et al. 2009) and was suggested to be connected with intensive persecution of wolves after In four areas (Ljubljansko barje-black, Bela Krajina-green, Krasred, and Zgornje Posočje-blue), the surveys were repeated in several years the second world war (Krofel et al. 2017), as well as longdistance movements of livestock herded by nomadic pastoralists (Brelih 1955). Lack of jackal records in Slovenia in 1960s and 1970s correspond with reduced occurrences elsewhere in Europe, which was attributed to widespread poisoning campaigns across South-eastern Europe (Giannatos et al. 2005;Krofel et al. 2017). Next expansion wave in Europe, which again reached Slovenia, was detected in the 1980s, following an all-time low of wolf populations in this part of Europe (Kryštufek & Tvrtković 1990, Krofel et al. 2017. Afterwards, the jackal numbers in Slovenia steadily increased, until around 2010, when we detected establishment of the first territorial groups. Since then, the number of new records increased exponentially (Fig. 2). This pattern suggests that in the first six decades the population dynamics in Slovenia was largely dependent on the development of source jackal populations in the Balkans and Pannonian basin. In contrast, after the establishment of first territorial groups and commencement of local reproduction, the population likely became increasingly self-sustaining in the last decade and less affected by developments in the   Female  2  1  3  Male  2  2  Unknown  3  3  2011-2017  Female  6  2  8  Male  13  3  16  Unknown  3  3  Entire study period Female  11  1  2  14  Male  23  3  26  Unknown 2  13  15  Total  36  4  15  55 1 3 neighbouring regions. Results of genetic analyses, including samples collected in Slovenia after 2005, suggest that jackals in this part of Europe originate from the recent expansions from the Caucasian region that spread through Pannonian basin and to a lesser extent from the remnant archaic populations along the Mediterranean coasts (Rutkowski et al. 2015;Stronen et al. 2021). Between 2006 and 2017, jackal surveys in Slovenia were largely conducted on voluntary basis and as part of student efforts (Fon 2017;Krofel 2009;Lamut 2020;Mladenović, 2016). Nevertheless, these surveys gave us insight into the development of jackal population during the critical period in Slovenia. The number of detected territorial groups of jackals was steadily increasing during the study period and similar is true for the proportion of calling stations with detected response in respect to the effort (response rates increased from 0% in 2006 to 20% in 2016; Fig. 3). Lower response rate in the final year (2017) was due to research focus on the Dinaric Mountains, where jackals were mostly absent, but several surveys were conducted there with the aim to understand occurrence of jackals in the wolf core areas (Fig. 4).
At the moment, our understanding of the population trends in Slovenia is best for the four regions where systematic surveys were repeated over several years (Ljubljansko barje, Kras, Zgornje Posočje, Bela Krajina). These data indicate that jackal densities are not the highest in areas, which were the first colonized by the species (i.e., Ljubljansko Barje and Zgornje Posočje), but in the area where the first reproductions were detected, i.e., Kras. On Ljubljansko barje, the densities stayed relatively stable since the establishment of first jackal territorial groups, while in Kras the relative density increased relatively fast, especially in the last years of the study (Fig. 5). The general increasing trend appears to have continued also after our study was completed, based on the data collected with camera trapping (Fležar et al. 2022;Krofel et al. 2022b), as well as the acoustic surveys performed by the local hunting clubs in 2017-2019 (Potočnik et al. 2018;Kraševec 2022).
While acoustic surveys provide a reliable indicator of relative population changes and comparison in the estimates of minimum density of territorial groups among different regions, data have to be interpreted with caution and cannot be used as an absolute measure of the population size  (Giannatos et al. 2005;Lamut 2020). Similar is true for opportunistically-collected data, which are prone to several potential biases. In our case, the effort for collection of this type of data stayed relatively constant between 2005 and 2017, which should reduce potential bias during this period (with exception of the mortality records, see below). Despite limitations, the general trends from all types of data we collected indicate similar population dynamics, which is also consistent with trends reported from across Europe (Krofel et al. 2017). Distribution pattern of golden jackals in Slovenia remained similar throughout the study period (Fig. 1), with jackals occurring mainly in the lowlands and fragmented landscapes outside of wolf core areas. Same pattern was reported in Slovenia also after our study was completed (Kraševec 2022) and is comparable to other regions in Europe (Šálek et al. 2014;Newsome et al. 2017;Ranc et al. 2018). Increase in jackal numbers and their distribution in Slovenia is paralleled with increasing trend in jackal-caused damages on livestock, which peaked in 2019 with 95 reported cases of jackal attacks and 23,438 € of compensations paid by the government (SIRENA 2023). However, due to potential for misidentification, data on jackal-caused damages should be treated with caution, if detection is not supported with genetic methods (Mihelič & Krofel 2012).
Because golden jackal was a novel and relatively unknown species in Slovenia, at first it received little interest from the authorities and its legal status remained unresolved for several years. The species had no legal status in the country before Slovenia entered the European Union in 2004. In this period, there was no regulation of hunting of jackals, which were regularly shot in small numbers, often confused for foxes. Between 2004 and 2014, the golden jackal was listed as a protected species, following its status under the Annex V in the Habitats Directive (Trouwborst et al. 2015). Mortality records in that period almost exclusively belonged to roadkills and only three shot animals were reported, which were at a time considered illegal killings. We assume the mortality rates obtained during 2004-2014 (Fig. 2) to be underestimated, since several more animals were probably shot, but not reported. With an increasing jackal population, also the interest for the species amongst stakeholders and authorities increased, mainly due to concerns of their impact on livestock and game species, especially European roe deer, similar to other countries in Europe (Ćirović et al. 2016). In 2014, golden jackal became listed as a game species, but no culling quotas were issued at first. Besides, the species also kept the status of protected species, mainly because no official systematic monitoring was established as required by the Habitats Directive for Annex V species (Trouwborst et al. 2015). Thus, the golden jackal was simultaneously listed as a protected and game species in Slovenia between 2014 and 2019. After an official national monitoring of the golden jackal conducted by hunters was established in 2018 (Potočnik et al. 2019), the legal protection status of golden jackal was removed in 2019 and legal hunting of jackals was initiated in 2020. During the first three years of the culling program, 154, 311, and 316 jackals were shot in 2020, 2021 and 2022, respectively (OSLIS 2023).

Conclusions
Due to its small size, Slovenia is unlikely to ever host an important part of the European jackal population. Nevertheless, due to its geographical position it could represent an important corridor for jackal expansion towards the north and west of the continent from the core areas in South-eastern Europe. Furthermore, the course of the jackal population development in Slovenia could serve as a model scenario for other Central and Western European countries with similar human densities and land use where jackal is currently absent or only occasionally detected.
Compared to the neighbouring regions in the Balkan peninsula and Pannonian basin that were experiencing exponential golden jackal population growth already in the 1990s and 2000s (e.g., Toth et al. 2009, Banea et al. 2012, Markov 2012, Ćirović et al. 2016, in Slovenia the substantial increase only started to occur in the 2010s, i.e., about 60 years after first arrival of the species and 30 years since regular presence in the country. When minimum densities of jackal territorial groups from our study in Slovenia are compared with data obtained with the same method elsewhere, densities are still considerably lower than values obtained from most other countries (Table 2).
Possible explanations for a slow population growth in the first phases of colonization and relatively lower abundance could be related with different waste management regime in the country, resulting in less organic waste, which represents an important food source for jackals in many parts of the South-eastern Europe (Ćirović et al. 2016) or a higher forest cover, which is a suboptimal habitat for golden jackal, especially where stable wolf packs are present (Šálek et al. 2014;Krofel et al. 2017;Newsome et al. 2017;Ranc et al. 2018). However, it also needs to be considered that expansion of jackals in Slovenia is not yet complete and that densities will likely continue to increase in the future. Thus, the observations from Slovenia appear to be more in accordance with the 'distance' hypothesis, although the environmental factors seem to also had a role in the development of this jackal population.
Our study demonstrates that jackals can successfully colonize and spread across a Central European country characterised by lower anthropogenic food resources compared to the South-eastern Europe. Important conclusion is also that exponential growth can occur even after a considerable time lag since the first appearance of the species and a long period (i.e. several decades) of only occasional presence. This could serve as a representative example of the jackal population development in other parts of Central Europe and beyond, where conditions are similar to Slovenia and where currently this mesocarnivore is present only sporadically or where first territorial jackal groups are currently being established.