New Data on the Occurrence of Scarabaeoid Beetles (Coleoptera: Scarabaeoidea) in Montenegro

Simple Summary The Montenegrin insect fauna is still insufficiently researched compared to neighbouring countries. The authors focus on scarabaeoid beetles. The dominant trophic group among scarabaeoid beetles are dung beetles. Dung beetles accelerate the decomposition of faeces, increase soil aeration and reduce parasite (flies and nematodes) numbers. Due to their role in nature, they are sometimes called meadow and forest scavengers. We collected 2130 scarabaeoid beetles belonging to 107 species and 5 families in 34 localities. Collected beetles constitute 54.2% of scarabaeoid beetles recognised so far from Montenegro. Among the fauna collected in this study, 63 species were dung beetles and 16 species were found in Montenegro for the first time. These included Odonteus armiger, Trox sabulosus, Ochodaeus integriceps, Agrilinus convexus, Melinopterus reyi, M. sphacelatus, Phalacronothus biguttatus, Trichonotulus scrofa, Psammodius nocturnus, Platytomus tibialis, Pleurophorus mediterranicus, P. pannonicus, Rhyssemus berytensis, Onthophagus ovatus, Rhizotrogus aestivus and Chaetopteroplia segetum. The discovery of so many species in a relatively short time of fieldwork indicates the need to continue and intensify our surveys in the future. Recommendations for the conservation of Montenegrin biodiversity are given. Abstract The Montenegrin fauna of the superfamily Scarabaeoidea is not satisfactorily studied. This is evidenced by the small number of species from this superfamily reported from Montenegro, despite the richness of the country’s habitats, especially high-mountain meadows, pastures, lush canyons, riverside, coastal dunes and old forests. Moreover, significant is the greater number of species of scarabaeoid beetles in neighbouring countries. Therefore, we aim to supplement the current information on the distribution of the taxa of the superfamily Scarabaeoidea in the country. The presented scarabaeoid beetles were caught during three expeditions: the first in May/June 2019, the second in May/June 2021, and the third in July 2021. As a result of this study, we have collected 2130 beetles belonging to 107 species and five families of the superfamily Scarabaeoidea: Geotrupidae, Trogidae, Lucanidae, Ochodaeidae and Scarabaeidae. The 28 days of the faunistic study confirmed the occurrence in Montenegro of 54.2% of the scarabaeoid species hitherto known from this country and added 16 new species that had not been previously recorded: Odonteus armiger (Scopoli, 1772), Trox sabulosus (Linnaeus, 1758), Ochodaeus integriceps Semenov, 1891, Agrilinus convexus (Erichson, 1848), Melinopterus reyi (Reitter, 1892), M. sphacelatus (Panzer, 1798), Phalacronothus biguttatus (Germar, 1824), Trichonotulus scrofa (Fabricius, 1787), Psammodius nocturnus Reitter, 1892, Platytomus tibialis (Fabricius, 1798), Pleurophorus mediterranicus Pittino & Mariani, 1986, P. pannonicus Petrovitz, 1961, Rhyssemus berytensis Marseul, 1878, Onthophagus ovatus (Linnaeus, 1767), Rhizotrogus aestivus (Olivier, 1789) and Chaetopteroplia segetum (Herbst, 1783). Six species and three subspecies that are typical for the Balkan Peninsula were also found: Trypocopris alpinus balcanicola (Mikšić, 1954), Onthophagus panici Petrovitz, 1964, Amphimallon solstitiale simplicissimum (Müller, 1902), Omaloplia illyrica (Baraud, 1965), Triodontella dalmatica (Baraud, 1962), Chaetopteroplia segetum straminea (Brullé, 1832), Anomala matzenaueri Reitter, 1918, Exomala adriatica (Petrovitz, 1968) and Oxythyrea dulcis Reitter, 1899. Thus, the number of currently known scarabaeoid species in Montenegro has increased to 184. Twenty-four species of scarabaeoid beetles are illustrated. Our results indicate insufficient knowledge of the Scarabaeoidea of Montenegro and, at the same time, their diversity and the presence of rare species among them. High-mountain and coastal communities of coprophagic scarabaeoid beetles, as well as communities of scarabaeoid beetles inhabiting coastal dunes, are especially valuable, worthy of protection. Therefore, further research and new expeditions to Montenegro are highly desirable.


Introduction
The Scarabaeoidea (scarabaeoid beetles) inhabit all zoogeographic regions of the world. They are the most species-rich in the tropics and the further north, the less numerous they become. In Europe, scarabaeoid beetles are represented by 8 families, 208 genera and ca. 1250 species [1]. A dominant trophic group among scarabaeoid beetles are dung beetles. Dung beetles are encountered worldwide, but they are particularly diverse in tropical forests and savannahs [2]. Evidence of fossil faeces clearly indicates that dung beetles had been connected with dinosaurs even before the mammals evolved [3]. Dung beetles can be endocoprid, paracoprid or telecoprid [4]. Endocoprid species lay eggs directly into the dung on the soil surface. Paracropid species dig tunnels beneath or nearby the dung, which end with brood chambers. Telecoprid species separate a portion of dung and transport it far from the original dung source, where the beetles bury in short to deep tunnels [5]. The diversified methods of dung transporting and foraging obviously result in an increased diversification of ecological processes such as nutrient recycling, soil aeration, plant seed dispersal, and reduction of parasite numbers, which provide benefits both to the ecosystem and to human activities [6]. Among the scarabaeoid beetles, there are also saproxylophagous, necrophagous, phyllophagous and rhizophagous species. There are forest and pasture species as well as mountain and lowland species; some of them are attracted by flowers or fermenting fruits, while others to artificial lights.
Taxonomic and faunistic works allow us to understand the behaviour of scarabaeoid beetles fully. Such works provide descriptions of new taxa and classify the organisms, and show their distribution, diversity, and habitat requirements. They constitute the basis for further research, e.g., on the relationships in dung beetles communities and their role in nature.
The Montenegrin fauna of the superfamily Scarabaeoidea is not sufficiently studied. The first comprehensive, relevant work was "Fauna Insectorum Balcanica-Scarabaeoidea", which included information on the occurrence of 97 species from this superfamily in Montenegro [7]. In the first appendix published by the same author, there are 112 species [8]. In the second appendix, Mikšić [9] lists another six species new to the fauna of Montenegro, but at the same time removes the two species mentioned in the first appendix. Consequently, the number of recorded scarabaeoid beetle species from Montenegro increased to 116. According to the "Katalog der Lamellicornia Jugoslawiens (Insecta-Coleoptera)", the number of scarabaeoid beetle species known from Montenegro was 122 [10].
The Catalogue of Palaearctic Coleoptera [11] contains one common list of Scarabaeoidea species for Montenegro and Serbia, while the second edition of the same catalogue contains two separate lists of scarabaeoid species for these countries. The second edition contains 163 scarabaeoid species (Geotrupidae-7 species, Trogidae-2, Lucanidae-5, Glaphyridae-1 and Scarabaeidae-148) from Montenegro [1]. There are 94 species of dung beetles among the Scarabaeoidea of Montenegro.
Most of the works on the Scarabaeoidea of Montenegro were published in the last century. Some of these works cover a much larger area than the present territory of Montenegro (e.g., the territory of the former Yugoslavia or the Balkan Peninsula). Consequently, many records have a rather general character without any precise locality data. With this research, we aim to supplement the current information about the distribution of the taxa of the superfamily Scarabaeoidea in the country. We also give advice on the protection of valuable scarabaeoid beetle communities.

Materials and Methods
The presented data are the result of three entomological expeditions. The collecting of scarabaeoid beetles was done between 27 June and 2 July 2019, next between 19 May and 2 June, and finally between 17 and 23 July 2021. We collected material in 34 localities (Table 1 and Figure 1) located in fifteen municipalities: Andrijevica (1 locality), Budva (2), Cetynia (2), Gusinje (3), Herceg Novi (1), Kotor (1), Kolašin (4), Mojkovac (3), Nikšić (4), Plav (1), Plužine (2), Podgorica (1), Rožaje (2), Ulcinj (4) and Žabljak (3).  Table 1). Figure 1. Collection localities of the scarabaeoid beetles in Montenegro (2019, 2021) (numbers of the localities correspond to those in Table 1). During the field studies, a variety of environments were searched and collecting methods were used. We looked for them on flowers, leaves of the trees and grass, on trunks of dead trees and in their hollows, in wood dust, litter, the upper layer of soil, as well as in remnants of dead animals, excrements of domestic and wild animals (e.g., cattles, horses, sheep, dogs, wild boars, foxes). We caught imagines in insect nets, insect sweep nets, insect beating sheets and traps baited with fresh sheep droppings. For psammophilous species, we sifted sand on seashore dunes and riverbanks and examined pieces of wood, stones lying there. Additionally, at night, we attracted insects to UV-illuminated screens and searched on trunks of old trees and their leaves using LED lights.
All The systematic arrangement and nomenclature were adopted from the Catalogue of Palaearctic Coleoptera [1]. Based on the publication of Nikolajev [12], the names of subgenera in the genus Trox Fabricius, 1775 were adopted. The authorship of the name of the species Anoplotrupes stercorosus has been changed based on the publication of Ziani et al. [13].     During the field studies, a variety of environments were searched and collecting methods were used. We looked for them on flowers, leaves of the trees and grass, on trunks of dead trees and in their hollows, in wood dust, litter, the upper layer of soil, as well as in remnants of dead animals, excrements of domestic and wild animals (e.g., cattles, horses, sheep, dogs, wild boars, foxes). We caught imagines in insect nets, insect sweep nets, insect beating sheets and traps baited with fresh sheep droppings. For psammophilous species, we sifted sand on seashore dunes and riverbanks and examined pieces of wood, stones lying there. Additionally, at night, we attracted insects to UV-illuminated screens and searched on trunks of old trees and their leaves using LED lights. All

Results
As a result of this study, 2130 beetles belonging to 107 species in five families of the superfamily Scarabaeoidea were collected: Geotrupidae (5 spp.), Trogidae (2 spp.), Lucanidae  (52 exx.). The most commonly observed species of pleurostict scarabaeoid beetles were: Cetonia aurata (13 localities) and Oxythyrea funesta (12 localities The list of the recorded species, along with their new localities, is presented below. Species new to the Montenegro fauna are marked with an asterisk (*).

List of Taxa
Superfamily SCARABAEOIDEA Latreille, 1802. Family GEOTRUPIDAE Latreille, 1802. Subfamily BOLBOCERATINAE Mulsant, 1842. *Odonteus armiger (Scopoli, 1772) ( Figure 5A).   Remarks. Reported from most European countries, including those around Montenegro (Albania, Bosnia Herzegovina, Croatia, Serbia), Armenia, Azerbaijan and Turkey [14][15][16][17]. Two individuals of this species were caught with an insect net. One of them was caught at dusk, on a dry and bushy pasture ( Figure 3B), the other one at night, on a small clearing in an oak forest ( Figure 4D) Remarks. Subspecies inhabiting Albania, Bosnia Herzegovina, Italy and Montenegro [16][17][18]. All individuals were caught on high mountain meadows with numerous tunnels dug by rodents (Figure 2A,C). In the morning and at noon, they were caught under the excrement of cows and horses, and in the afternoon, they walked quickly on the meadow.  [19][20][21]. All individuals were caught on high mountain meadows (Figure 2A,B and Figure 4B). Males and females of this species were caught under the old excrement of dogs and foxes and sheep wool lying on the ground.
Family  [22]. All individuals of this species were caught with an insect net. They flew at dusk and in the early night among tall reeds adjacent to the coastal dunes ( Figure 4G) Remarks. Known from many European countries (including Montenegro's neighbours: Albania, Bosnia Herzegovina, Croatia, Serbia), as well as Armenia, Azerbaijan and Georgia. Recorded also in Iran, Mongolia, Asiatic Russia (East and West Siberia, Far East), Turkey, Algeria, Morocco and Tunisia [17,[23][24][25]. Imagines were caught in sheep, cow and horse dung in mountain pastures (over 900 m above sea level) (Figure 2A,D,E,H and Figure 3F).
Amidorus Remarks. Mediterranean species are known from five countries in Africa (Algeria, Egypt, Libya, Morocco, Tunisia) and six countries in Europe (Albania, Italy, Malta, Montenegro, Portugal, Spain) [25,26]. Found in Albania and Montenegro for the first time in 2015 [26]. One individual of this species was caught in the dung of a cow on a pasture. This is the second record from Montenegro.
Melinopterus consputus (Creutzer, 1799) [25,27]. All individuals of this species were caught in cow dung lying on the road near the river ( Figure 3A). Remarks. Known from many European countries (including Montenegro's neighbours: Albania, Bosnia Herzegovina, Croatia, Serbia), as well as Armenia, Azerbaijan and Georgia. Reported in Asia from Iraq, Israel, Kazakhstan, Kyrgyzstan, Russia (East and West Siberia), Turkey, Turkmenistan, and from North Africa in Algeria, Morocco and Tunisia [25]. Imagines were caught in cow and horse dung on mountain pastures (over 900 m above sea level) (Figure 2A,D,E,H and Figure 3G *Phalacronothus biguttatus (Germar, 1824) ( Figure 6A).   [25]. Collected from underneath sheep droppings on pastures (Figures 3C,G and 4A,B).
Phalacronothus quadrimaculatus (Linnaeus, 1760). Remarks. Known from many European countries (including Montenegro's neighbours: Albania, Bosnia Herzegovina, Croatia, Serbia), as well as Armenia and Georgia. Reported from Kazakhstan, Asiatic Russia (West Siberia), Turkey, Algeria, Morocco and Tunisia [25]. Montenegro, it is found only in Bosnia and Herzegovina. In Asia, reported from Cyprus, Iran, Turkey and Uzbekistan [32]. All the specimens were caught in the afternoon on the sidewalk in a holiday resort located by the sea ( Figure 4H). They were caught in an insect sweep net. *Rhyssemus berytensis Marseul, 1878 ( Figure 6I) Remarks. In Europe, it is only known in Bulgaria and Greece (Macedonia) [32,33]. Outside Europe, it is reported in Cyprus, Iran, Iraq, Israel, Lebanon and Turkey. Individuals of this species were observed in the evening between 5 p.m. and 8 p.m. Most of them were found on the sidewalk in a holiday resort located by the sea, and single ones between the roots of grasses growing on seashore dunes ( Figure 4F,H)  Remarks. Recorded from Balkan Peninsula: Albania, Bosnia Herzegovina, Greece, North Macedonia and Montenegro [24,35,36]. Imagines have been gathered on high mountain pastures with numerous tunnels dug by rodents (Figure 2A-C,E): most of them in ground-trapped using fresh sheep droppings for bait, the rest of them directly in sheep droppings, rarely in cows and horse's faeces. Remarks. Reported from most European countries, including those around Montenegro (Albania, Bosnia Herzegovina, Croatia, Serbia) and also Azerbaijan, Georgia, Iran, Kazakhstan, Tajikistan and Turkey [34,35]. Imagines were caught on pastures at an elevation of about 600 to 1000 m above sea level, all from the excrement of sheep, cows and horses ( Figure 3B-F).
The 28 days of faunistic study resulted in confirming the occurrence in Montenegro of 54.2% of the scarabaeoid species hitherto known from this country and added 16  Six species and three subspecies that are typical for the region of Balkan Peninsula were also found: Trypocopris alpinus balcanicola, Onthophagus panici, Amphimallon solstitiale simplicissimum, Omaloplia illyrica, Triodontella dalmatica, Chaetopteroplia segetum straminea, Anomala matzenaueri, Exomala adriatica and Oxythyrea dulcis. These species were observed at single localities.
The diversity of scarabaeoid fauna on the Balkan Peninsula suggests that this number may be increased further. Kulundžić et al. [48] estimated that more than 400 scarabaeoid species occur in Croatia, while Guéorguiev et al. [49] estimated the number of scarabaeoid species in Bulgaria at 335-345. As regards the adjoining countries, 240 scarabaeoid species are currently known from Croatia, 214 from Kosovo and Serbia, 204 from Bosnia Herzegovina [1] and 201 from Albania [17]. In the first edition of the "Catalogue of Palaearctic Coleoptera" [11], there are 156 scarabaeoid species mentioned from Albania. Ten years later, its second edition [1] already listed 181 species, and 3 years later, the number of species reached 201 [17].

Conclusions
Within less than a month of fieldwork, the discovery of 16 species new to Montenegro also points to the insufficient state of knowledge of its scarabaeoid fauna. Hence, there is a need to continue and intensify faunistic studies, especially in the hitherto less explored areas. The diversity of the scarabaeoid fauna of Montenegro is certainly greater. Among the 107 species of scarabaeoid beetles observed during our field studies, 63 of them are coprophagous. Montenegro is a European country where, due to the traditional form of grazing, dung beetle communities are characterised by a considerable richness of species and the presence of rare species. Three important aspects for the conservation of dung beetle diversity emerge from this work: saving the traditional form of domestic animal grazing, law for the protection of well-preserved pastures and active protection in order to ensure adequate living conditions for rare species. The third of the above-mentioned aspects is also important for preserving beetle communities inhabiting the Montenegrin coastal dunes. Recommended protection of dung beetles should be based on maintenance and introduction of small-size herds of goats and sheep, single cows and horses on mountain pastures. Then, the protection of psammophilous scarabaeoid beetles should include the removal of garbage from coastal dunes and the prevention of these habitats from being overgrown by shrubs and trees. Equally important is the possibility of conducting further research on the structure of these communities. The importance of the traditional grazing system and the importance of long-term research were clearly demonstrated by Tretler et al. [52]. The cited authors found that as much as 51% of Sardinian coprophagic scarabaeoid beetles occur on the small Asinara island (only 51.9 km 2 ).