Dung-beetles (Coleoptera, Scarabaeidae, Aphodiinae, Scarabaeinae) feeding on faeces of steppe marmots Marmotabobak (Rodentia, Sciuridae) in Middle Volga territory

Abstract Background In open terrestrial biomes of Holarctic realm, ground squirrels are recognised as keystone species inhabiting steppes. They shape the plant species composition and diversity and support a fauna of species associated with their burrows. Ground squirrels and associated dung-beetles are important elements of the steppe food webs, yet the trophic associations between species are still poorly studied. New information The area in the northern outskirts of Obshchy Syrt plateau, on the border of Samara and Orenburg Provinces of Russia was surveyed and scarab beetles (Scarabaeidae) feeding on steppe marmot (Marmotabobak (Müller, 1776)) faeces were collected from six localities. Twenty eight species of two subfamilies – Aphodiinae and Scarabaeinae, - were identified with the majority of species belonging the genus Aphodius Hellwig, 1798. Seven species are recorded as consumers of marmot faeces for the first time. Only two nidicolous specialist species were found which suggests that the studied population of steppe marmots is as result of the recent secondary colonisation and not all the associated scarab beetle faunas were re-established.


Introduction
The concept of keystone species has become established in ecology and conservation research, although the term "keystone species" has varied meanings in literature (Mills et al. 1993).In the most general meaning, keystone species are those which presence is crucial for maintaining the diversity of their ecological communities and which importance is disproportionally large relative to their abundance (Paine 1969).In the open terrestrial biomes of the Holarctic realm, ground squirrels of the tribe Marmotini Pocock, 1923, are commonly recognised as keystone species inhabiting steppes (Lindtner et al. 2020, Lindtner et al. 2018).Large ground squirrels of the genus Marmota Blumenbach, 1779, comprise 15 species.The species of this genus were a subject of long-lasting research because of their importance and, also, as the main carriers of plague in some areas.
A nidicolous fauna associated with burrows of ground squirrels was studied by a number of authors.The scarab beetle fauna inhabiting marmot burrows in Russia is dealt with in a few studies (Egorov 1997, Zinchenko and Nemkov 1998, Zinchenko 2003).Two new species of the genus Aphodius, A. isajevi Kabakov, 1994 andA. exilimanus Kabakov, 1994, were described in the past decades from marmot burrows (Kabakov 1994) and they are considered specialist nidicolous.However, these studies were focused on the documentation of the fauna found in the borrows and not on the trophic associations of beetles and marmots.
Recently, we conducted field research in Bol'shechernigovskij District, Samara Province and the Pervomaiskij District, Orenburg Province, European Russia.The area is inhabited by steppe marmot (Marmota bobak (Müller, 1776)).As a result of the survey, a large number of dung-beetle species were registered feeding on the steppe marmot excrements.The goal of the present contribution is to report the registered trophic associations of scarab beetles with steppe marmots and discuss, based on the associated beetles fauna, the possibility of native versus introduced origin of this marmot population.

Collecting localities
The collecting area is situated some 520 km north of the Caspian Sea coast, in the Pontic steppe ecozone (Fig. 1).The six sampling localities are situated mostly between crop fields with outermost localities separated by about 10 km (Fig. 2).The characterisation of the localities is given in Table 1 and habitat illustrations are given in Figs 3,4,5,6,7.

Material collecting and deposition and data presentation
Beetles were collected in latrines near marmot burrow entrances.The beetles were picked up from faeces and upper soil layer beneath faeces with a forceps and placed in tubes with Table 1.
Characterisation of the collecting localities.

Distribution
This species is widely distributed in Europe, occurs also in the Caucasus, the Transcaucasus, Turkey, Kazakhstan and Turkmenistan.In Russia, it is known from the steppe zone from Kursk Prov. to West Siberia.

Biology
In Russia, the species occurs in rodent burrows (mostly of marmots and sousliks).In some localities, beetles can be found in large numbers near burrow entrances in May-June (Isajev 1995).However, in the UK, this species was collected under vegetable debris and sheep, cow and horse dung (Jessop 1986).It was also collected from rabbit latrines (Jason Mate, pers.comm.)Probably, in west Europe, in the areas without Marmotini rodents, this species develop in burrows of other rodents or rabbits, but its life cycle needs further research.

Distribution
The species is distributed in central, south and eastern Europe, the Transcaucasus, Asia Minor, Kazakhstan and Turkmenistan.In Russia, it is known from Ulyanovsk and Novosibirsk Provinces, Volgograd, Rostov, Orenburg Provinces and Krasnoyarsk Terr.

Biology
The species occurs in open biotopes, in marmot holes and in the dung of domestic animals.

Distribution
The species occurs in central and eastern Europe, north and eastern Kazakhstan, Kyrgyzstan.In Russia, it is known from the European part and West Siberia (up to Krasnoyarsk in the north-east).

Biology
The beetles and larvae feed on horse dung.

Distribution
The species is distributed in the steppe zone of central and eastern Europe and Kazakhstan.

Biology
A nidicolous steppe species occurring in gopher and marmot holes.

Distribution
The distribution range of this species includes the whole of Europe (except for the extreme north), North Africa, the Transcaucasus, Asia Minor, Kazakhstan, Middle Asia, Mongolia.It was imported to North America.In Russia, it occurs throughout the country in the European part, reaching Baikal Region in the east.

Biology
The species occurs in cow and horse dung, in marmot holes and also is attracted to light.In Russia, the beetles are active from March to October.It is a common, locally abundant species.

Distribution
The species occurs in Europe (except for the extreme north), west, middle and Central Asia; it was imported to North America.In Russia, it is distributed throughout the country.

Biology
This eurybiont species is abundant throughout its range occurring mostly in open biotopes, in the dung of domestic and wild animals.

Distribution
The species is widely distributed in Europe, North Africa, Kazakhstan, Middle and Central Asia, imported to North America and Australia.In Russia, it occurs throughout the country up to Eastern Siberia in the east.

Biology
In

Distribution
The species is distributed throughout Europe (except for the extreme north), west Asia, Kazakhstan and Middle Asia; imported to North America.In Russia, it occurs from the western border up to Transbaikal Region.

Biology
The species is common in all the parts of its range.

Distribution
The distribution range of this species includes the whole of Europe, North Africa, the Caucasus, the Transcaucasus, Kazakhstan, Middle Asia, Afghanistan, Mongolia, north and south-western China, the Korean Peninsula and Japan; it was imported to North America.In Russia, it is distributed throughout the country.

Biology
The species mostly occurs in cow and horse dung, in open biotopes.

Distribution
The species occurs throughout Europe, in Morocco, Egypt, the Caucasus, the Transcaucasus, Asia Minor, Syria, Kazakhstan, middle and Central Asia.In Russia, it occurs from the western borders up to southern Yakutia.

Biology
The species is common in the major part of its range and prefers open biotopes.The beetles feed on horse, cow and donkey dung; they are attracted to light and occur from April to September.

Distribution
The species occurs in Europe, North Africa, the Transcaucasus, Asia Minor, Kazakhstan, the mountains of Middle Asia; it was imported to North America.In Russia, it is distributed throughout the European part and occurs in south of West Siberia.

Biology
A coprophagous species feeding on cow, horse, donkey and sheep dung.

Distribution
The species occurs in central, south and eastern Europe, North Africa, west Asia, Kazakhstan and Middle Asia.In Russia, it is distributed from the western border to Transbaikal Region, mostly in the steppe zone and the forest-steppe subzone of the deciduous forest zone.

Biology
The species occurs in open biotopes, in the dung of domestic animal and in marmot holes.On the territory of Russia, the beetles are active from March to October.The species is common throughout its range.

Distribution
The species occurs throughout Europe, in North Africa (Morocco, Algeria), the Caucasus, the Transcaucasus, Asia Minor, Syria, Lebanon, Israel, Kazakhstan, middle Asia and Mongolia; it was imported to USA and Canada.In Russia, it is distributed from the western border to Yakutia.

Biology
A coprophagous species feeding on dung of cows, horses and wild ungulates.In Russia, this species is common; in southern regions, it occurs from March to December.Dung-beetles (Coleoptera, Scarabaeidae, Aphodiinae, Scarabaeinae) feeding ...

Distribution
The species is distributed in Europe, except for the extreme north, North Africa (Morocco, Tunisia), the Trancaucasus, west Asia, Kazakhstan and Middle Asia.In Russia, it is common in the European part, reaching the Transbaikal Region to the east.

Ecology
The species occurs in the dung of domestic animals and in marmot holes.

Distribution
The distribution range of this species includes almost the whole of Europe (except for the extreme north), the Caucasus, the Transcaucasus, Kazakhstan, Middle Asia, Asia Minor, Mongolia, north China, Korean Peninsula and Japan.In Russia, it is distributed throughout the country.

Biology
It is a common, locally abundant species feeding on cow, horse and sheep dung.

Distribution
The species is distributed in Europe, North Africa, west Asia, Kazakhstan and Middle Asia.In Russia, it mostly occurs in the Vorga Region and the Ciscaucasus.

Biology
A coprophagous species occurring in the dung of different animals.It prefers arid biotopes with sandy and sandy clay soils.

Distribution
The species is widely distributed in central and south Europe; it is also known from North Africa, the Transcaucasus, Asia Minor, Syria and Turkmenistan.In Russia, it is known from Samara and Astrakhan Provinces.

Biology
The species occurs in cow dung.

Distribution
The species occurs in central andeEastern Europe, the Transcaucasus, Middle Asia.In Russia, it is mainly distributed in northern Caucasus and the Volga Region.

Biology
The species occurs in cow and horse dung, mostly in open biotopes.

Distribution
The species occurs in Europe (up to Finland in the north), North Africa (Morocco), the Caucasus, the Transcaucasus, Asia Minor, Kazakhstan, Middle Asia, Afghanistan, Mongolia, China, North Korea.It was imported to Canada and the USA.In Russia, the species is mostly distributed in the forest-steppe subzone of the deciduous forest zone from the western border to the Amur Region.

Biology
A coprophagous species occurring in ungulate dung.

Distribution
The distribution range of this species includes central and southern Europe, North Africa, the Transcaucasus, Asia Minor, Kazakhstan and Middle Asia.In Russia, it is mostly distributed in the steppe zone and forest-steppe subzone of the zone of deciduous forest from the western border to South Siberia.

Biology
The species occurs in diverse biotopes, in cow and horse dung and in riverside debris.

Onthophagus (Palaeonthophagus) semicornis (Panzer, 1798) Distribution
The species is distributed in southern part of western and central Palaearctic.

Ecology
The species mostly occurs in steppe biotopes.A generalist coprophage, feeding on ungulate dung, faeces of rodents and birds.

Distribution
The species is distributed in southern and middle Europe, northern Africa, Asia Minor and Iranian Plateau.

Biology
A common, sometimes abundant generalist coprophage feeding mostly on cattle, horse and sheep dung.

Distribution
The species is widely distributed in the southern Palaearctic.

Biology
The species mostly occurs in steppe and semi-desert biotopes.A generalist coprophage, feeding mostly on ungulate dung.

Distribution
The species is distributed in southern Europe, Asia Minor and western Central Asia.

Biology
A generalist coprophagous species feeding mostly on cattle and horse dung.

Analysis
The collected specimens belonged to 28 species of two coprophagous subfamilies -Aphodiinae and Scarabaeinae (Table 2).The former subfamily was represented by the genus Aphodius and comprised majority of species.Scarabaeinae comprised seven species of four genera.Onthophagus was represented by four species, while Caccobius, Euoniticellus and Sisyphus -by one species each.The number of species per locality varied significantly, from 22 species in locality 6 to only three in locality 2. Of the 28 species encountered, only two Aphodius species belonged to specialist nidicolous, associated with ground squirrels, while the great majority belong to generalist coprophages which apparently do not utilise marmot faeces as a primary food source (but see below regarding O. leucostigma).Seven species were not previously recorded as consumers of marmot faeces.

Discussion
In the open terrestrial biomes of the Holarctic realm, ground squirrels of the tribe Marmotini are commonly recognised as keystone species, having a major impact on their ecological communities.Burrow-dwelling rodents are considered ecosystem engineer species in steppes where they shape the plant species composition and diversity (Valkó et al. 2021).
It was demonstrated that the European ground squirrel Spermophilus citellus (Linnaeus, 1766) helps to maintain heterogeneity in temperate grassland ecosystems (Lindtner et al. 2020, Lindtner et al. 2018).Ground squirrels are a focal group for conservation efforts in many countries (Caro 2010).
There exists a nidicolous fauna of insects that are associated with burrowing rodents and live in their burrows.One of the prominent components of this fauna are the Scarabaeidae dung beetles that feed on rodent faeces and those larvae develop inside the burrows.Zunino and Halffter (2007)  In studying of the association between burrowing rodents and scarab beetles, one should distinguish between trophic association and development association.The former implies that a certain beetle species feeds on excrements of a certain rodent species.It may be a specialist coprophage, feeding only on excrements of one species or that prefers faeces of a certain rodent species, but may occasionally feed on faeces of other animals and last, but not least a generalist coprophage that feeds on faeces of different animals occurring within its range.Development association refers to specialist nidicolous species that depend, during at least one of its development stage, on the presence of the rodent species and cannot develop without its burrows.In this respect, feeding of a beetles species on the rodent faeces does not necessarily mean that it is a nidicolus species and, vice versa, a species found inside a burrow did not necessarily came to the burrow attracted to rodent faeces.
The present study is focused on the trophic association of scarab beetles and steppe marmots.During the survey, we encountered a reasonably large number of dung beetle species attracted to steppe marmot faeces.Most of these species, 26 of 28, belong to generalist coprophages (Table 2).
Several researchers studied beetles, including Scarabaeidae, associated with Marmota species and collected from inside burrows or immediately near burrow openings.For example, two specialist nidicolous species of Aphodius, A. isajevi Kabakov, 1994 andA. exilimanus Kabakov, 1994, were described from steppe marmot burrows in similar steppe biotopes in southern Ul'yanovsk Province, Russia, some 230 km NW of the survey area (Kabakov 1994).These beetles were collected in the same period as our survey (second half of May) and Isajev (1995) noted that both species were rather common and locally abundant, but only occurred in native colonies of steppe marmots; they were not found in the colonies of re-introduced marmot.
The exact status of the examined colonies of steppe marmot is not clear.Bibikov et al. (1990) wrote that before the increased anthropogenic pressure, steppe marmots were abundant in steppe biotopes in Russia but, due to almost continuous ploughing of native steppes and unrestricted hunting, the species was almost exterminated in Russia by the beginning of the 20 century.In 1970s-1990s, steppe marmots were re-introduced in large territories of its former range, including the southern part of Samara Province (Bibikov et al. 1990). Naumov et al. (2013) wrote that, by the 1950s in Samara Province, native colonies of the steppe marmot existed in a few distant areas, including Bol'shechernigovskij District, but noted that the detailed information about the distribution of the species at that time is lacking.After a comprehensive survey of the steppe marmot in Samara Province, they found a metapopulation with 22 colonies and 118 families in Bol'sheglushitskij and Bol'shechernigovskij Districts.They also concluded that the majority of the colonies were at the earlier stages of the introduction (Naumov et al. 2013).
Our results are congruent with the above-mentioned; however they are somewhat intermediate between the results that previous researchers reported for native and reacclimatised colonies of steppe marmots.The fauna of the associated dung-beetles in the surveyed area did not include only generalist coprophages, as was previously reported for all studied re-acclimatised colonies (Isajev 1995, Egorov 1997).We found two specialist nidicolous species of Aphodius, A. arenarius and A. citellorum, in locality 4, but they were represented by only one and six specimens, respectively.We also found O. leucostigma in locality 5.This species is not apparently strictly nidicolous, but is known to prefer living in burrows of ground squirrels (Carpaneto andPittino 1998, Kabakov 2006).Therefore, we did not encounter the fauna characteristic for native marmot colonies in terms of both abundance and species richness.Available data (e.g.Frolov and Akhmetova (2013), Isajev (1995)) suggest that nidicolous species of Aphodius are rather common or abundant in suitable habitats.Provided that the marmot colonies are native, in the studied area, one would expect at least a few other nidicolous species, namely A. rotundangulus, A. isajevi, A. exilimanus and O. vitulus.
It should be noted that the surveyed area lies within distribution ranges of two souslik species, Spermophilus pygmaeus (Pallas) and S. major (Pallas) (Dudnikov et al. 2022), which potentially can support nidicolous fauna.They were, however, not encountered during our study.
Our results suggest that the steppe marmot colonies in the surveyed area are a result of a recent (apparently a few decades old) dispersion from southern regions with stable th Dung-beetles (Coleoptera, Scarabaeidae, Aphodiinae, Scarabaeinae) feeding ... populations.Further monitoring of the nidicolous species will probably show re-establishing of the fauna associated with marmots and support the assumption of the important role of ground squirrels in biodiversity of the steppe biotopes as well as agricultural lands.
In the present contribution, we also report our findings about trophic associations of beetles and marmots as a set of nanopublications.Nanopublications are small data containers represented by named RDF graphs that can be automatically interpreted and aggregated (Kuhn et al. 2016).One of the possible uses of nanopublications in biodiversity is communicating new information in a standardised way (Dimitrova et al. 2021).We think that such nanopublication may be especially useful in accumulating and analysing data in food webs research.
reviewed the information of associations of Onthophagus Latreille, 1802, species with vertebrate burrows and reported a reasonable number of species associated with marmots and ecologically similar rodents.Similar synoptic studies for Aphodiinae or Aphodius Hellwig, 1798, are not available, but considering that Aphodiinae, especially the mega-diverse genus Aphodius, dominate dung-beetle communities in the many regions where ground squirrels are distributed, it is expected a similarly diverse nidicolous Aphodius fauna.