Biology and seasonal population dynamics of the forest dung beetle Anoplotrupes stercorosus (Coleoptera: Geotrupidae) in the Center of European Russia

. The biology and population dynamics of Anoplotrupes stercorosus was studied in forest ecosystems of central European Russia (2007-2023). During the study period, 6738 individuals were collected from 256 habitats. In open biotopes, Anoplotrupes stercorosus was caught only occasionally or no specimens were found at all. The species is most abundant in mixed forests with a pronounced shrub layer and grass cover, complex pine forests and deciduous forests. Seasonal population dynamics varies in different habitats. It can be with one, two or three population peaks. The possibility of using Anoplotrupes stercorosus as a bioindicator of forest ecosystem condition was studied. The abundance of the species was found to be very low on burned areas.


Introduction
There is a variety of reasons causing the loss of biodiversity and the extinction of insect species in many parts of the planet in recent years [1][2][3][4].They include habitat fragmentation, changes in climatic conditions and associated effects, fires, droughts, floods, chemical pollution, urbanisation, deforestation, and introduction of invasive species [5][6][7][8].Coleoptera are one of the most important groups of insects.In all ecosystems they are an important component of the fauna [9][10][11].The superfamily Scarabaeoidea numbers over 35,000 species worldwide [12].In Europe, Scarabaeoidea are represented by 8 families, 208 genera and about 1,250 species [13].Species of the family Geotrupidae are ubiquitous.Representatives of four subfamilies can be found in the Palaearctic: Athyreinae, Bolboceratinae, Lethrinae and Geotrupinae.The subfamily Geotrupinae is represented in the Palaearctic by 17 genera and 218 species, of which 61 occur exclusively in Europe [13].
The dung beetle is the dominant trophic group among the Scarabaeoidea.They are found all over the world, but are particularly diverse in tropical forests and savannahs.There are forest and grassland species as well as mountainous and lowland species.Their action as saproxylophagous and necrophagous ensures the transformation of decomposing wood, plant and animal residues and the integration of organic matter into the nutrient cycle.Beetles of the family Geotrupidae are particularly diverse in their food specialisation [14][15][16].
The forest dung beetle Anoplotrupes stercorosus (Scriba, 1791) is a species widely distributed in Europe, the Caucasus and western Siberia.In Russia, it is the most widespread and most abundant representative of the forest-dwelling family Geotrupidae [17,18].Its larvae feed on leaf litter buried 25-30 cm deep by imagos.Such substrate, buried for larval feeding, enriches the deeper mineral layers of the soil with organic material.This is particularly important in pine forests, which usually grow on poor sandy soils.Imagos feed on a wide variety of organic residues: decaying organic remains, leaf litter, animal droppings, decaying fungal fruiting bodies and fermented tree sap [19,20].
More recently, Geotrupidae have been seen as indicators of environmental conditions.The possibility of using Anoplotrupes stercorosus to monitor forest ecosystems has been described in several publications [19,21,22].Thus, data on abundance and abundance of this species can be used to analyse the condition of forest ecosystems.At the same time, knowledge about its biology in different parts of its range is still poorly known.The aim of the study is therefore to investigate the biology of the species in central European Russia.
To determine whether Anoplotrupes stercorosus could be used as an environmental indicator, we used data on the seasonal population dynamics of this species in soil traps at 8 plots that differed from each other.Collections were made in 2022 in the Republic of Mordovia using pitfall traps placed in a line of 10 at a distance of 2 m in a line.The plot 1 was affected by fires of 2010.After these fires, there are many standing and fallen dry pine and birch trees on the plot.Birch trees and shrubs have started to appear.The birch trees are growing close to each other.Shrubs are mainly represented by raspberries.Grass layer is sparse.Small birch leaf litter.It was not exposed to fires in 2021 and is 0.5km from the boundary of the 2021 fires.Plot 2 was affected by fires in 2010 and 2021.It is located 2 km from the fire edge into the burnt area.The area burned completely in 2021.The intense fire destroyed the grass layer, shrubs, growing birch, and dead wood.The open sandy surface makes up approximately 95% of the area of the plot.In 2022, the herbaceous layer started to recover slightly.Plot 3 is similar to plot 1.However, it is 10 m away from the fires of 2021.Plot 4 is adjacent to plot 3 (10 m deep into the area of fires of 2021).The plot burned in 2010 and 2021.After the 2021 fires, the open sandy surface takes approximately 90% of the area of the plot.In 2022, the herbaceous layer began to recover slightly.Plot 5 is completely identical to plot 2, but is located 1 km from the fire edge deep into the burned area.Plot 6 is located on the 2010 and 2021 burned areas.It is located 10 m from the fire edge into the burnt area (20 m from plot 7).After the fires of 2010, dry pines were left on this plot and birch forest started to grow actively.But in 2021, the birch forest, bushes and herbaceous layer burned partially.At present, there is deadwood and dense dry birch forest on the plot.The grass cover has started to recover.Plot 7 is a control plot of forest that has not been exposed to fire.It is located 10 m from the fire edge.Old-growth mixed forest of pine, birch with admixture of linden (in the first tier), mountain ash, birch, bird cherry (in the second tier).The litter is well-pronounced and thick.Grass layer is sparse.Plot 8 is a control plot of forest that was not exposed to fire.The plot is located 0.5 km from the fire edge.It is an old-growth mixed forest of pine, birch with a mixture of linden (in the first tier), mountain ash, birch, and bird cherry (in the second tier).The litter is well-pronounced and thick.Grass layer, due to lack of light, is poorly expressed and sparse.
The distribution and abundance of Anoplotrupes stercorosus in different biotopes was assessed using a scale of six points: 0 -the species does not occur in this habitat type; 1 -the species occurs as solitary specimens in less than 50% of all studied plots, not occurring in others; 2 -the species is not numerous, numbers up to 5 specimens, in less than 50% of all studied plots, occurs in single specimens in the majority of surveyed localities; 3 -the species is common in less than 50% of all studied plots, numbers between 5 and 50 specimens in the majority of studied plots; 4 -the species is numerous in less than 50% of all studied plots, numbers between 50 and 100 specimens in the majority of studied plots; 5 -the species is numerous in the majority of studied plots (over 50%), numbers over 100 specimens.Biotopes were distinguished on the basis of several features: open (without woody vegetation) and closed biotopes.Open biotopes were distinguished by moisture, anthropogenic pressure, soils and proximity to forest ecosystems.Closed (forested) biotopes differed in woody vegetation and origin of forest areas.
The seasonal dynamics of Anoplotrupes stercorosus abundance was studied in 2015 in different forest ecosystems differing in moisture, presence of herbaceous and shrub tier, and forest forming species.Collections were made using pitfall traps placed in a line of 10 at a distance of 1.5 m in a line.Numbers were determined as dynamic density (in individuals per 100 trap days).

Results
A total of 6738 Anoplotrupes stercorosus specimens were collected from traps in 256 biotopes (Table 1).In some open biotopes, in spite of the large number of studied plots, only a few or no Anoplotrupes stercorosus specimens were recorded.Therefore, the beetle abundance estimate at these plots was very low (0 or 1).At the same time, we recorded beetles near forested areas in pitfall traps.This was especially relevant for forested glades, which are surrounded by forest ecosystems.In forest ecosystems of various types, abundance and occurrence numbers of Anoplotrupes stercorosus are higher than in open ecosystems.The species is most abundant in mixed forests with a well-defined shrub layer and herbaceous cover, complex pine forests, and deciduous forests.
The abundance of Anoplotrupes stercorosus differed in the studied and control plots in mixed forest depending on the degree of fire damage.For example, in plot 2, which was 2 km from the fire edge deep in the burnt area, not a single specimen was caught during the whole season.At the same time, in the control plots (plot 7 and plot 8) the abundance of the species was maximum during the whole season, as Figure 1 shows it accounted for 8.7 and 20.4 individuals per 100 trap days, respectively.The seasonal dynamics of the Anoplotrupes stercorosus population in these plots showed different peaks under different conditions.In plot 8 (control), for example, two abundance peaks were detected in late May-June and in the second half of July.However, a slight increase in abundance was observed in late September/early October (Fig. 2).In plot 7, population peaks were found in late July-August and September.The seasonal dynamics of the species was almost absent in the burned places along with lower numbers of Anoplotrupes stercorosus.Based on the average values for all plots, three population peaks can be distinguished: late May-June, late July-August and September.However, it should be noted that the differences in seasonal abundance patterns among plots were significantly different from each other.Thus, the clearest peaks in abundance were recorded only at the three plots, which were located next to untouched forest or in the mixed forest.
In untouched forest ecosystems, abundance patterns were mainly with a single peak that occurred in July and early August (Fig. 3).The only exception was in the wet deciduous forest, where the maximum abundance of Anoplotrupes stercorosus was recorded in the second half of May.

Discussion
Anoplotrupes stercorosus is the most widespread and abundant representative of the family Geotrupidae in the forests of central European Russia [17,18].In open ecosystems, this species is less abundant than in closed forest ecosystems.For example, in meadow steppes and dry steppe biotopes with open areas of soil, it has never been recorded in soil traps.It is also rare in agrosystems and in dry and wet floodplain meadows.However, near forest ecosystems Anoplotrupes stercorosus is beginning to be detected regularly in soil traps.Similar preferences have been identified in studies in Italy and the Czech Republic.The species preferred forest ecosystems and was very rarely found in grasslands, despite similar lures [25][26][27].Similar results were obtained during our studies in 2022 on burned plots (Fig. 1).In plots that burned completely in 2021, the abundance of Anoplotrupes stercorosus was very low compared to an old-growth mixed forest.
Anoplotrupes stercorosus is considered a shade-loving species, preferring deciduous plant communities and occurring less frequently in alder forests.Most researchers conclude that high groundwater levels make the biotop unfavourable for Anoplotrupes stercorosus as they negatively influence larval development [28].Such unfavourable conditions with increased moisture levels are typical for alder forests and some deciduous forests in lowland areas.In our studies, the highest numbers of Anoplotrupes stercorosus were recorded in mixed forests, various deciduous forests and pine forests with well-defined tiering.Larvae are known to feed mainly on plant debris, while imagos are found both on plant debris, decaying fungi, animal droppings, and dead animal carcasses [19,20,26,29] In this context, it is clear that a good litter layer (decaying leaves) is essential for the life cycle of Anoplotrupes stercorosus.
Other studies in Europe show that Anoplotrupes stercorosus is almost exclusively caught in forests where it is the most dominant species [30,31].Similar studies reported significant catches of this species in traps set in pine forests in southern Poland.Moreover, its abundance in all forest plots is almost identical.Even in areas affected by fires and subsequently planted with young pines, Anoplotrupes stercorosus numbers were high [32].In Romania, this species also dominates forests among all Geotrupidae [33].
Anoplotrupes stercorosus is known from various publications to avoid wet forest areas.For example, Byk and Semkiw [19] showed that alder forest was one of the least suitable habitats for the species.This is due to the high level of groundwater in alder forests, which prevents reproduction and larval development.On the other hand, Marczak and Mroczynski [31] observed high numbers of Anoplotrupes stercorosus in other alder forests with relatively lower groundwater levels.Apparently, Anoplotrupes stercorosus is a species that can adapt quickly to changing environmental conditions.The data on its presence in burned plots, where its abundance is quite high, confirm the ability of the species to adapt to different conditions [32,our data].Byk [34] proved that Anoplotrupes stercorosus is widespread in stands found in post-agricultural areas.By infesting stands in mass numbers on postagricultural land, the beetles modify soil characteristics and accelerate the development of forest soils.
Our data show that Anoplotrupes stercorosus occurs very frequently and in high numbers in mixed forests with a well-defined shrub layer and herbaceous cover, complex pine forests, deciduous forests.Similar results have been obtained in different parts of its range [30][31][32][33][34][35][36][37].There are reports that a higher content of fine sand in forest soils had a positive effect on the abundance of Anoplotrupes stercorosus.Sand improves oxygen penetration into the soil, which increases the breeding and development opportunities of the species [29].Anoplotrupes stercorosus plays a very important role in the decomposition of forest litter, plant residues, leaves and wildlife litter.In pine forests, this function of the beetle is irreplaceable [38].According to data from Voronezh Region, Anoplotrupes stercorosus has peaks in June-July and September [39].In the National Park Belovezhskaya Pushcha, Anoplotrupes stercorosus peaked in mid-May and mid-July [36].Klimaszewski & Strużyński [40] found relatively high and constant numbers of individuals of the species from mid-May to mid-August with a significant increase in abundance in mid-June.However, the highest number of individuals was observed in mid-September and early October.Marczak [41] studied the abundance of Anoplotrupes stercorosus in a pine forest and observed an increase in numbers in July and September.
We assume that differences in the seasonal dynamics of Anoplotrupes stercorosus abundance between the studied forest types are due to unequal microclimatic conditions and humidity.In our studies in humid forests, the highest peaks in abundance were found in May, when the forests are still quite humid.In contrast to our results, Marczak and Mroczynski [31] showed that Geotrupidae appear relatively late in relatively wet alder forests, which flood before early May.Moreover, only one clear peak in abundance was observed in such conditions, during the warmest and driest period of the year.We suppose that in our biotopes warm spring caused the occurrence of Anoplotrupes stercorosus, since it provided rapid warming of soil in the forest.This, in turn, facilitated rapid emergence of imagos.In pine forests with a well-developed grass layer and shrubs, numbers of Anoplotrupes stercorosus are rather high until late September and October.

Conclusion
During the studies, 256 biotopes located in open and forested ecosystems were examined.In open biotopes single specimens of Anoplotrupes stercorosus were recorded or no specimens were found at all.The species is most abundant in mixed forests with a well-defined shrub layer and grass cover, complex pine forests and deciduous forests.The possibility of using Anoplotrupes stercorosus as a bioindicator of forest ecosystems was studied.The seasonal dynamics of the population varies in different biotopes.It may be with one, two or three population maxima.We assume that these differences are caused by unequal microclimatic conditions and moisture content.In our studies in humid forests, the highest population peaks were found in May, when the forests are still quite wet.

Table 1 .
Conventional distribution and abundance of Anoplotrupes stercorosus in different biotopes (based on 2007-2022 data).