Biodiversity Data Journal :
Taxonomy & Inventories
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Corresponding author: Lilia A. Akhmetova (akhmetova@scarabaeoidea.com)
Academic editor: Lyubomir Penev
Received: 09 Apr 2024 | Accepted: 23 May 2024 | Published: 18 Jun 2024
© 2024 Lilia Akhmetova, Andrei Kurochkin, Andrey Frolov
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Akhmetova LA, Kurochkin AS, Frolov AV (2024) Dung-beetles (Coleoptera, Scarabaeidae, Aphodiinae, Scarabaeinae) feeding on faeces of steppe marmots Marmota bobak (Rodentia, Sciuridae) in Middle Volga territory. Biodiversity Data Journal 12: e125090. https://doi.org/10.3897/BDJ.12.e125090
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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.
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 (Marmota bobak (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.
steppe marmot, ground squirrels, keystone species, scarab beetles, dung-beetles, coprophagy
The concept of keystone species has become established in ecology and conservation research, although the term “keystone species” has varied meanings in literature (
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 (
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.
The collecting area is situated some 520 km north of the Caspian Sea coast, in the Pontic steppe ecozone (Fig.
No |
Photo |
Locality |
Date |
Coordinates |
Characterization |
1 |
Fig. |
Bol’shechernigovskij Distr., 2.44 km SSW of Polyanskij Vill. |
19.05.2023 |
|
A patch of forb-fescue-feather grass steppe with a colony of steppe marmots with more than 10 living burrows, located on an almost flat area and surrounded by forest belts and agricultural fields. |
2 |
Fig. |
Bol’shechernigovskij Distr., 3.53 km SSW of Polyanskij Vill. |
19.05.2023 |
|
A patch of forb-grass steppe with a rather large colony of steppe marmots with more than 15 living burrows, located on the slopes of the gullies and on the intergully spaces; the gully system is surrounded on all sides by agricultural fields. |
3 |
Fig. |
Bol’shechernigovskij Distr., 3.54 km SSW of Polyanskij Vill. |
28.04.2023 |
|
Same as No 2. |
4 |
Fig. |
Bol’shechernigovskij Distr., 3.9 km SSW of Polyanskij Vill. |
28.04.2023 |
|
A patch of forb-grass steppe with a small colony of steppe marmots on an almost flat, extended gully slope, with less than a dozen living burrows without pronounced hills of soil, which is a part of the population from localities 2 and 3. |
5 |
Fig. |
Pervomaiskij Distr., 6.28 km SSW of Polyanskij Vill., urochishche Pal’govo |
18.05.2023 |
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A patch of forb-fescue steppe with a small colony of steppe marmots along the bottom and lower part of the slope of a gully surrounded by agricultural fields. |
6 |
Pervomaiskij Distr., 7.32 km SSW of Koshkin Vill., urochishche Pal’govo |
19.05.2023 |
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A patch of forb-wormwood-grass steppe with a few burrows on the slope of a gully near the top; the area is surrounded by agricultural field, except for northwest, where it borders the Talovskaya Steppe Cluster Area of the Orenburg Nature Reserve. |
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 ethanol. Individuals, arriving at faeces during survey, were also collected. All collected material is housed the the Zoological Institute RAS, Saint-Petersburg, Russia (ZIN).
Classification, distribution and biology of Aphodiinae species follow
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.
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 (
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.
The species occurs in open biotopes, in marmot holes and in the dung of domestic animals.
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).
The beetles and larvae feed on horse dung.
The species is distributed in the steppe zone of central and eastern Europe and Kazakhstan.
A nidicolous steppe species occurring in gopher and marmot holes.
The distribution range of this species includes almost the whole of Europe (except for the extreme north), the Transcaucasus, Asia Minor, west Kazakhstan and Tajikistan. In Russia, the species is known from Leningrad, Nizhny Novgorod, Voronezh, Saratov, Volgograd and Astrakhan Provinces.
A coprophagous species occurring in the dung of cows, horses and wild ungulates. The species occurs in different biotopes: in eastern Europe, in forests;
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.
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.
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.
This eurybiont species is abundant throughout its range occurring mostly in open biotopes, in the dung of domestic and wild animals.
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.
In Russia, imagoes are active from April to October occurring in open biotopes, pastures, in cow, sheep and horse dung.
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.
The species is common in all the parts of its range. It occurs in open biotopes in the dung of different animals, in carrion and in marmot holes.
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.
The species mostly occurs in cow and horse dung, in open biotopes.
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.
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.
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.
A coprophagous species feeding on cow, horse, donkey and sheep dung.
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.
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.
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.
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.
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.
The species occurs in the dung of domestic animals and in marmot holes.
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.
It is a common, locally abundant species feeding on cow, horse and sheep dung.
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.
A coprophagous species occurring in the dung of different animals. It prefers arid biotopes with sandy and sandy clay soils.
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.
The species occurs in cow dung.
The species occurs in central andeEastern Europe, the Transcaucasus, Middle Asia. In Russia, it is mainly distributed in northern Caucasus and the Volga Region.
The species occurs in cow and horse dung, mostly in open biotopes.
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.
A coprophagous species occurring in ungulate dung.
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.
The species occurs in diverse biotopes, in cow and horse dung and in riverside debris.
The species is distributed in southern part of western and central Palaearctic.
The species mostly occurs in steppe biotopes. A generalist coprophage, feeding on ungulate dung, faeces of rodents and birds.
The spcies is widely distributed in the Palaearctic Region, introduced in North America. In Russia, it occurs throughout the European part, in West and Central Siberia.
A generalist coprophagous species feeding mostly on cattle dung. It was also registered feeding on carrion and rotten food.
A western Palaearctic species. In Russia, it is common in the central and southern European part, reaching southern Urals Mountains in the east.
A generalist coprophagous species feeding mostly on cattle dung.
Southern Ukraine, southern European Russia up to Volga Basin in the east, north-western Kazakhstan.
A nidicolous species inhabiting burrows of steppe rodents. It was also registered feeding on sheep and cattle dung.
The species is distributed in southern and middle Europe, northern Africa, Asia Minor and Iranian Plateau.
A common, sometimes abundant generalist coprophage feeding mostly on cattle, horse and sheep dung.
The species is widely distributed in the southern Palaearctic.
The species mostly occurs in steppe and semi-desert biotopes. A generalist coprophage, feeding mostly on ungulate dung.
The species is distributed in southern Europe, Asia Minor and western Central Asia.
A generalist coprophagous species feeding mostly on cattle and horse dung.
The collected specimens belonged to 28 species of two coprophagous subfamilies – Aphodiinae and Scarabaeinae (Table
Dung-beetle species |
Localities |
Trophic associations |
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1 |
2 |
3 |
4 |
5 |
6 |
Generalist coprophagous species |
Specialist nidicolous, associated with rodents |
Previous records of trophic association with Marmota sp. |
|
Aphodius arenarius |
+ |
+ |
+ |
||||||
Aphodius biguttatus |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Aphodius bimaculatus |
+ |
+ |
|||||||
Aphodius citellorum |
+ |
+ |
+ |
||||||
Aphodius coenosus |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Aphodius distinctus |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
|
Aphodius erraticus |
+ |
+ |
+ |
+ |
+ |
||||
Aphodius fimetarius |
+ |
+ |
|||||||
Aphodius granarius |
+ |
+ |
+ |
||||||
Aphodius haemorrhoidalis |
+ |
+ |
+ |
||||||
Aphodius immundus |
+ |
+ |
+ |
||||||
Aphodius luridus |
+ |
+ |
+ |
+ |
+ |
||||
Aphodius melanostictus |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
||
Aphodius prodromus |
+ |
+ |
+ |
||||||
Aphodius punctatosulcatus |
+ |
+ |
+ |
||||||
Aphodius pusillus |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Aphodius quadriguttatus |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
||
Aphodius quadrimaculatus |
+ |
+ |
+ |
||||||
Aphodius satellitus |
+ |
+ |
+ |
+ |
|||||
Aphodius scrofa |
+ |
+ |
+ |
+ |
|||||
Aphodius varians |
+ |
+ |
|||||||
Caccobius schreberi |
+ |
+ |
+ |
||||||
Euoniticellus fulvus |
+ |
+ |
|||||||
Onthophagus leucostigma |
+ |
+ |
+ |
||||||
Onthophagus nuchicornis |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Onthophagus semicornis |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
+ |
|
Onthophagus vacca |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Sisyphus schaefferi |
+ |
+ |
+ |
+ |
+ |
+ |
|||
Total: 28 |
12 |
3 |
10 |
18 |
22 |
8 |
26 |
2 |
21 |
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 (
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.
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
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 and A. 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 (
Similar results were obtained by
The exact status of the examined colonies of steppe marmot is not clear.
Our results are congruent with the above-mentioned; however they are somewhat intermediate between the results that previous researchers reported for native and re-acclimatised 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 (
It should be noted that the surveyed area lies within distribution ranges of two souslik species, Spermophilus pygmaeus (Pallas) and S. major (Pallas) (
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 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 (
We are thankful to Jason Mate, Sergei Tarasov, Dirk Ahrens, Tobias Kuhn and Lyubomir Penev for reading the draft and providing the comments that improved our work. A.S. Kurochkin gratefully acknowledges I.V. Sharonova (Samara University, Samara) for help during fieldwork in Samara and Orenburg Provinces and for providing characteristics of plant communities of the beetle collection sites. The insect collection of ZIN is maintained within the framework of the Russian State research project 122031100272-3.