applied sciences

Article Effect of Granulometric Composition of the Soil on the Occurrence of Carrion Beetles (Coleoptera: Silphidae)

Karolina Konieczna 1,*, Zbigniew W. Czerniakowski 1 and Małgorzata Szostek 2

1 Department of Agroecology and Forest Utilization, College of Natural Sciences, University of Rzeszów, Cwikli´nskiej1,´ 35-601 Rzeszów, Poland; [email protected] 2 Department of Soil Science, Environmental Chemistry and Hydrology, College of Natural Sciences, University of Rzeszów, Zelwerowicza 8B, 35-601 Rzeszów, Poland; [email protected] * Correspondence: [email protected]

Abstract: The entomological material was collected in the years 2009–2012 and 2014 from 13 different habitat types from three localities in south-eastern Poland. In total, 11,095 Silphidae were collected. This study examined whether the percentage of individual soil granulometric fractions was signif- icantly related to the total abundance of collected Silphidae and individual carrion beetle species. A positive correlation and a statistically significant correlation were found between the total number of specimens collected and the share of the mechanical fraction with a diameter of 0.05–0.002 mm (silt fraction). In three species, a statistically significant correlation was demonstrated between the number of collected Silphidae and the share of the mechanical fraction with a diameter of 2–0.05 mm (sand fraction). The two species Phosphuga atrata atrata and Nicrophorus vespilloides the correlation was positive. A statistically significant relationship was also observed for Thanatophilus sinuatus, but the correlation was negative. With regard to the mechanical fraction with a diameter <0.002 mm (clay fraction), a statistically significant relationship was demonstrated for Oiceoptoma thoracicum and


for Nicrophorus vespilloides for which the correlation was negative. However, a positive correlation
 was found for T. sinuatus in this case. Citation: Konieczna, K.; Czerniakowski, Z.W.; Szostek, M. Keywords: Silphidae; carrion beetles; soil; granulometric composition; correlation Effect of Granulometric Composition of the Soil on the Occurrence of Carrion Beetles (Coleoptera: Silphidae). Appl. Sci. 2021, 11, 1017. https:// 1. Introduction doi.org/10.3390/app11031017 Taxa of epigeic insects belonging to the carrion beetle family (Coleoptera: Silphidae) are associated with the presence of carrion [1–3], which constitutes a valuable but unstable Received: 10 December 2020 source of nutrients for them. Carrion is usually subjected to rapid changes under the Accepted: 19 January 2021 Published: 23 January 2021 influence of biotic (scavenger animals, bacteria, and fungi) and abiotic (e.g., temperature and humidity) factors. Therefore, rapid burying of carcasses by carrion beetles reduces

Publisher’s Note: MDPI stays neutral potential competitors [4,5] and preserves food. with regard to jurisdictional claims in Soil granulometric composition is an important parameter of the soil of the habitat published maps and institutional affil- and is a key factor regulate soil physical properties. Content of sand, silt, and clay fraction iations. regulate water movement, bulk density, porosity, plasticity, etc. For example, smaller particles (clays) having higher specific surface area than sand particles. These surfaces hold water through adhesion, exchange nutrients, and provide surfaces to which organic matter can attach. Sandy soils (>90% sand) have low specific surface area, resulting in large pores and high infiltration rates, whereas clay soils (>60% clay) have high specific surface area, Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. resulting in small pores and low infiltration rates [6]. This factors can extremely affected This article is an open access article occurrence of carrion beetles [7–9]. distributed under the terms and As demonstrated by Muths [7], the rate of carcass burying is influenced by many conditions of the Creative Commons factors of which soil structure and moisture are of particular importance. For the occur- Attribution (CC BY) license (https:// rence and reproductive success of insects belonging to the subfamily Nicrophorinae, the creativecommons.org/licenses/by/ physical properties of the soil appear to be of particular importance, especially for small 4.0/). species [1,8–10]. These species tend to prefer loose, moist soils rich in organic matter that

Appl. Sci. 2021, 11, 1017. https://doi.org/10.3390/app11031017 https://www.mdpi.com/journal/applsci Appl. Sci. 2021, 11, 1017 2 of 13

are easier to penetrate. In such soils it is possible to bury carrion quickly and effectively. If the soil is too dense, insects cannot penetrate it. However, it need attention that soil that is too loose may not maintain the form of a hole (brood chamber—in the case of Nicrophorinae), leading to its burial and suffocation [11]. In turn, larger species prefer open areas where the soil is drier and sandier [8]. These relationships prompted us to undertake a closer examination of the relationship between the number of collected Silphidae (Silphinae and Nicrophorinae) and the physical parameters of the soil, in particular the percentage of soil mechanical fractions.

2. Materials and Methods 2.1. Research Area The study was carried out in various habitats of south-eastern Poland in 2009–2012 and 2014. The sites were located in Borek Stary (UTM EA73), Rzeszów (UTM EA74) and Widna Góra (UTM FA13/FA23) on 13 research localities (Table1; Figure1).

Table 1. Geographical characteristics, habitats, years of investigations, and numbers of samples at study area.

Locality Geographical Habitat Study Site Years Number of Samples * [UTM] Coordinates Borek Stary 49◦5604900 N mid-field balk a No. 1 2009/2010 44/48 [EA 73] 22◦60800 E Borek Stary 49◦5604200 N mid-field tree stand I No. 2 2009/2010 44/48 [EA 73] 22◦602000 E Borek Stary 49◦5605400 N mid-field tree stand II No. 3 2009/2010 44/48 [EA 73] 22◦604500 E Rzeszów 49◦5905900 N osier plantation No. 4 2011/2012 44/44 [EA 74] 22◦103500 E Rzeszów 49◦59056 N cluster of trees and shrubs No. 5 2011/2012 44/44 [EA 74] 22◦104300 E Rzeszów 50◦00900 N urban park No. 6 2011/2012 44/44 [EA 74] 22◦105300 E Widna Góra 49◦5902900 N mid-field balk b No. 7 2014 48 [FA13] 22◦4002500 E Widna Góra 49◦5903500 N mid-field balk c No. 8 2014 48 [FA23] 22◦4002900 E Widna Góra 49◦5903500 N mid-field balk d No. 9 2014 48 [FA23] 22◦4003000 E Widna Góra 49◦5902900 N potato crop No. 10 2014 48 [FA13] 22◦4002400 E Widna Góra 49◦5903500 N fodder beet crop No. 11 2014 48 [FA23] 22◦4002800 E Widna Góra 49◦5903500 N cereal crop No. 12 2014 48 [FA23] 22◦4003000 E Widna Góra 49◦5903600 N backyard orchard No. 13 2014 48 [FA23] 22◦4002800 E a—mid-field balk between cereal crop and pasture, b—mid-field balk between potato crop and meadow, c—mid-field balk between fodder beet crop and cereal crop, d—mid-field balk between cereal crop and meadow, *—one sample constituted the content of one pitfall trap at one study site. Appl.Appl. Sci.Sci. 2021, 1111, x FOR PEER REVIEW 3 of 13 2021, , 1017 3 of 13

FigureFigure 1. 1.Location Location of research of research stands stands (Own work (Own out work based outon https://upload.wikimedia.org/wikipedia/commons/6/6e/ based on https://upload.wikimedia.org/wikipedia/com- Podkarpackie_mapa_fizyczna.pngmons/6/6e/Podkarpackie_mapa_fizyczna.png).).

The research sites sites were were located located in in Borek Borek Stary Stary covered covered habitats habitats in areas in areas used used for forag- agriculturericulture but but excluded excluded from from direct direct management management (wasteland). (wasteland). There There were were two two types types of ofmid mid-field-field trees trees (site (sitess 2 and 2 and 3) and 3) and mid mid-field-field balks balks (an (anunplowed unplowed strip) strip) separating separating the cul- the cultivationtivation of a of mixture a mixture of cereals of cereals and and pasture pasture (site (site 1). 1). InIn RzeszRzeszów,ów, carrioncarrion beetlesbeetles werewere collectedcollected atat threethree sites.sites. InIn suburbansuburban areas,areas, i.e.,i.e., inin anan area withwith aa greatergreater degreedegree ofof urbanization,urbanization, thethe selectedselected researchresearch sitessites includedincluded woodedwooded sites:sites: Salix viminalis osier plantation (site(site 4),4), aa cluster ofof trees andand shrubsshrubs (site(site 5),5), andand aa citycity parkpark (site(site 6).6). The researchresearch sites sites in in Widna Widna G óGóra,ra, like like in Borekin Borek Stary, Stary, were were located located in agricultural in agricultural areas. However,areas. However, these sites these were sites used were economically used economically and included: and included: a potato a Solanumpotato Solanum tuberosum tu- cultivationberosum cultivation (site 10), (site the cultivation 10), the cultivation of Beta vulgaris of Beta, semi-sugarvulgaris, semi type-sugar of fodder type of beet; fodder Zentaur beet; PolyZentaur variety Poly (site variety 11), Avena(site 11), sativa Avena, Hordeum sativa, vulgareHordeum, Triticum vulgare aestivum, Triticumcultivated aestivum forcultivated forage (sitefor forage 12), and (site a backyard12), and a orchardbackyard (site orchard 13). Additionally, (site 13). Additionally, the study coveredthe study the covered mid-field the balksmid-field adjacent balks to adjacent the above-mentioned to the above-mentioned crops (site crops 7, 8, and (site 9). 7, 8, and 9). 2.2. Analysis of Soil Granulometric Composition 2.2. Analysis of Soil Granulometric Composition Soil samples were collected at all test sites and air dried after been brought to lab- Soil samples were collected at all test sites and air dried after been brought to labor- oratory in room temperatures (21 ◦C) by 2 weeks. The granulometric composition was atory in room temperatures (21 °C) by 2 weeks. The granulometric composition was ana- analyzed using the hydrometer method [12,13]. The division of soils into granulomet- lyzed using the hydrometer method [12,13]. The division of soils into granulometric sub- ric subgroups was based on the recommendations of the United States Department of groups was based on the recommendations of the United States Department of Agricul- Agriculture (USDA) [14]. ture (USDA) [14]. 2.3. Collection of Entomological Material 2.3. Collection of Entomological Material Modified Barber traps (Figures2 and3) were used for catching the adult carrion beetlesModified (Coleoptera: Barber Silphidae). traps (Figure Fours 2 trapsand 3) were were set used up f onor catching the test sites the adult and were carrion dug bee- in linetles ( withColeoptera: the soil Silphidae). surface. Containers Four traps were were filled set up one-third on the test with sites ethylene and were glycol dug solution. in line Appl.Appl. Sci. Sci. 20 2120,21 11, ,11 x , FORx FOR PEER PEER REVIEW REVIEW 4 4of of13 13

Appl. Sci. 2021, 11, 1017 4 of 13

withwith the the soil soil surface. surface. C ontainersContainers were were filled filled one one-third-third with with ethylene ethylene glycol glycol solution. solution. The The trapstraps were were covered covered with with a aplastic plastic lid lid to to prevent prevent excessive excessive contamination contamination from from rain rain and and The traps were covered with a plastic lid to prevent excessive contamination from rain and vegetationvegetation (e.g. (e.g., falling, falling leaves). leaves). On On the the roof, roof, a baita bait was was attached attached with with a wire,a wire, it itconsisted consisted vegetation (e.g., falling leaves). On the roof, a bait was attached with a wire, it consisted ofof pieces pieces of of chicken chicken weighing weighing about about 100 100 g. g.The The trap trap was was additionally additionally surrounded surrounded with with a a of pieces of chicken weighing about 100 g. The trap was additionally surrounded with a metalmetal mesh mesh to to prevent prevent predat predatorsors (e.g. (e.g., foxes,, foxes, cats, cats, dogs, dogs, and and birds) birds) from from eating eating the the bait bait metal mesh to prevent predators (e.g., foxes, cats, dogs, and birds) from eating the bait andand destroying destroying them. them. Holes Holes in in the the metal metal mesh mesh were were approximately approximately 2 cm,2 cm, which which allowed allowed and destroying them. Holes in the metal mesh were approximately 2 cm, which allowed the beetles to pass into the trap with bait without thereby affecting the catchability of the thethe beetles beetles to to pass pass into into the the trap trap with with bait bait without without thereby thereby affecting affecting the the catchability catchability of of the the insects. The same type of bait was used at each site, with an average weight of 100 g. The insects.insects. TheThe samesame type type of of bait bait was was used used at at each each site, site, with with an anaverage average weigh weightt of 100 of 100g. The g. research was carried out from May to October. The traps were emptied on average every Theresearch research was was carried carried out outfrom from May May to October. to October. The Thetraps traps were were emptied emptied on average on average every two weeks, and the preservative fluid was changed and a new bait was put out. The cap- everytwo weeks, two weeks, and the and preservative the preservative fluid fluid was waschanged changed and anda new a new bait baitwaswas put putout. out. The Thecap- tured entomological material was then analyzed. capturedtured ento entomologicalmological material material was was then then analyzed. analyzed.

Figure 2. Diagram of the Barber trap used in the study (authors). FigureFigure 2. 2.Diagram Diagram of ofthe the Barber Barber trap trap used used in inthe the study study (authors) (authors). .

Figure 3. The Barber trap used in osier plantation Salix viminalis (authors). FigureFigure 3. 3.The The Barber Barber trap trap used used in in osier osier plantation plantationSalix Salix viminalis viminalis(authors). (authors).

2.4.2.4.2.4. Nomenclature Nomenclature Nomenclature and and and Statistical Statistical Statistical Analysis Analysis Analysis TheTheThe systematic systematicsystematic and and nomencla nomencla nomenclaturetureture of of the of the thecarrion carrion carrion beetles beetles beetles were werewere adopted adopted adopted in in accordance accordance in accor- withdancewith the the with study study the by studyby Löbl Löbl byand and Löbl Löbl Löbl and [1 [15 Löbl],5 ],and and [15 the ],the andbeetles beetles the were beetles were identified identified were identified according according according to to Mrocz- Mrocz- to kowMroczkowskikowskiski [16] [16] and and [16 Šustek ]Šustek and Šustek[17]. [17]. [17]. ToToTo assess assess assess the the biodiversity biodiversity ofof of thethe the collectedcollected collected entomological entomological entomological material, material, material, the the the Brillouin Brillouin Brillouin species sp spe-e- ciesdiversitycies diversity diversity index index index (H),ˆ (Ĥ), (Ĥ), the the the MargalefMargalef Margalef index index (biodiversity (biodiversity (biodiversity index) index)index) and and and domination domination domination index index index (D (D =( D1=- 1Simpson =-Simpson 1-Simpson index) index) index were were) were used. used. used. These These These analy analy analysessesses were were were performed performed performed using using using PAST PAST PAST 1.93 1.93 software 1.93 software soft- [18].ware[18]. The [The18 ].dominance dominance The dominance classes classes classes were were adopted were adopted adopted from from Górny from Górny G andó andrny Grüm andGrüm Grüm[19]. [19]. [ 19]. AA Achi chi-square chi-square-square test test test for for for the the the signi significance significanceficance of of of the the the association association association was was was provided. provided. provided. The The The normality normality normality ofofof the thethe distributions distributionsdistributions was waswas verified verifiedverified using using the the the Shapiro Shapiro Shapiro–Wilk–Wilk–Wilk test. test. test. Based Based Based on on the on the theobtained obtained obtained re- re- sults,results,sults, a decisiona a decision decision was was was made made made to to toselect select select a specifica specific specific type type of ofof test: test:test: parametric parametricparametric or oror non non-parametric.non-parametric.-parametric. TheTheThe impact impact impact of of of environmental environmental environmental variables variables variables on on on beetle beetle beetle assemblages, assemblages, assemblages, which which which included included included physical physical physical parameters (weight percentage of individual fractions in earth parts) was determined by using two tests. Pearson’s linear correlation test (r Pearson) was used for the analysis of Appl. Sci. 2021, 11, 1017 5 of 13

the examined traits with normal distribution. In the case the distributions of the examined features deviated from the normal, the non-parametric Spearman rank correlation. All the necessary analyses were performed in the PQStat ver. 1.8.0.488 (PQStat Soft- ware 2020, Pozna´n,Poland) and Statistica 10 software package (Statistica software V 10.0, StatSoft Inc., Tulsa, USA). PQStat Statistical Program version 1.6.2 [20] and Statistica 10 software [21]. The significance level (the maximum permissible probability of making a type I error) was set at α ≤ 0.05.

3. Results 3.1. Soil Granulometric Composition The results of the granulometric composition for soil samples from the test areas are presented in Table2 and Figure4. The following mineral deposits were found: (i) silt loam (SiL)—sites 1–5, 7–11, and 13; (ii) silty clay-loam (SiCL)—site 12; and (iii) sandy loam (SL)—site 6.

Table 2. Division of mineral deposits into granulometric subgroups according to the percentage of sand, silt and clay fractions of soil samples taken from test stands.

Sites Fractions Proportion of Fractions [%] Texture (USDA) sand (2–0.05 mm) 16 Site 1 silt (0.05–0.002 mm) 75 silt loam (SiL) clay (<0.002 mm) 9 sand (2–0.05 mm) 19 Site 2 silt (0.05–0.002 mm) 71 silt loam (SiL) clay (<0.002 mm) 10 sand (2–0.05 mm) 26 Site 3 silt (0.05–0.002 mm) 71 silt loam (SiL) clay (<0.002 mm) 3 sand (2–0.05 mm) 39 Site 4 silt (0.05–0.002 mm) 58 silt loam (SiL) clay (<0.002 mm) 3 sand (2–0.05 mm) 33 Site 5 silt (0.05–0.002 mm) 53 silt loam (SiL) clay (<0.002 mm) 14 sand (2–0.05 mm) 56 Site 6 silt (0.05–0.002 mm) 43 sandy loam (SL) clay (<0.002 mm) 1 sand (2–0.05 mm) 17 Site 7 silt (0.05–0.002 mm) 65 silt loam (SiL) clay (<0.002 mm) 18 sand (2–0.05 mm) 16 Site 8 silt (0.05–0.002 mm) 67 silt loam (SiL) clay < 0.002 mm 17 sand (2–0.05 mm) 19 Site 9 silt (0.05–0.002 mm) 66 silt loam (SiL) clay < 0.002 mm 15 sand (2–0.05 mm) 10 Site 10 silt (0.05–0.002 mm) 75 silt loam (SiL) clay < 0.002 mm 15 sand (2–0.05 mm) 13 Site 11 silt (0.05–0.002 mm) 66 silt loam (SiL) clay (<0.002 mm) 21 Appl. Sci. 2021, 11, x FOR PEER REVIEW 6 of 13

Appl. Sci. 2021, 11, 1017 6 of 13 silt (0.05–0.002 mm) 15 clay (< 0.002 mm)

sand (2–0.05 mm) Table 2. Cont. 13 Site 11 silt (0.05–0.002 mm) 66 silt loam (SiL) Sitesclay (< Fractions 0.002 mm) Proportion of21 Fractions [%] Texture (USDA)

sandsand 2– (2–0.050.05 mm) mm) 15 15 Site 12Site 12 siltsilt (0.0 (0.05–0.0025–0.002 mm) mm) 54 54 siltysilty clay clay loam loam (SiCL) (SiCL) clay (<0.002 mm) 31 clay (< 0.002 mm) 31

sand (2–0.05 mm) 14 sand (2–0.05 mm) 14 Site 13 silt (0.05–0.002 mm) 75 silt loam (SiL) Site 13 75 silt loam (SiL) silt clay(0.05 (<0.002–0.002 mm) mm) 11 clay (< 0.002 mm) 11

Figure 4 4.. UnitedUnited States States Depa Departmentrtment ofof Agriculture Agriculture (USDA (USDA)) soil soil textural textural triangle triangle.. Soil Soilsamples samples from from individualindividual research research sites sites are are marked marked with with triangles triangles [14]. [14 ].

3.2. Silphidae Species Species Composition Composition Figure 55 shows the the five five year year (200 (2009–2012,9–2012, and and 2014) 2014) beetle beetle collection collection numbers. numbers. A total A total of 11,095 carrion carrion beetles beetles were were collected. collected. The obtained specimens were classified into 13 species and 5 genera, which according to Löbl and Löbl [15], account for 59% of the Polish Silphidae fauna. In total, 876 samples were analyzed. Statistically significant differences were found between the number of specimens caught at individual sites (p < 0.05). However, no differences in the number of species were found (p = 0.9828). Selected parameters of α-diversity and the results of fauna analysis for the sites, which were not included in the studies of Konieczna et al. [20,21] (sites 4 and 13), are presented in Table S1 and Figure S1. The Brillouin diversity index (H),ˆ which is more sensitive to the overall sample size than the Shannon–Weaver index, ranged from 0.752 to 1.991 at the examined sites. The values of the Margalef’s diversity index, calculated on the basis of the natural logarithm (ln), ranged from 1.136 to 2.073 at the examined sites. Conversely, the dominance index ranged from 0.156 (site 2) to 0.628 (site 10). Appl. Sci. 2021, 11, 1017 7 of 13 Appl. Sci. 2021, 11, x FOR PEER REVIEW 7 of 13

FigureFigure 5. Box5. Box plots plots of of Silphidae Silphidae recorded recorded in in allall investigatedinvestigated sites. The The thick thick horizontal horizontal lines lines within within the the boxes boxes indicate indicate medianmedian values. values. On On each each box, box, the the bottom bottom and and top top edges edges of theof the box box indicate indicate the the 25th 25th and and 75th 75th percentiles, percentiles, respectively. respectively. Small Small black circles are outliers. black circles are outliers. The obtained specimens were classified into 13 species and 5 genera, which according 3.3.to Löbl Influence and Löbl of Soil [15] Granulometric, account for Composition59% of the Polish on the Silp Occurrencehidae fauna. of Silphidae In total, 876 samples wereThe analyzed. weight percentageStatistically ofsignificant sand, silt, differences and clay fractionswere found in the between soil at the individual number of sites wasspecimens varied andcaught statistically at individual significant sites (p ( χ< 20.05).= 171.05, However, DF = 24,no differencesp < 0.000001). in the By number means ofof the correlationspecies were test found we verified (p = 0.9828). the presence of a relationship between the percentage content of individualSelected fractions parameters and of the α total-diversity number and of the harvested results ofSilphidae, fauna analysis and whether for the there sites, was awhich relationship were not between included the percentagein the studies content of Konieczna of individual et al. fractions [20,21] (site ands the4 and abundance 13), are of individualpresented Silphidaein Table S1 species and Figure (Table S1.3). The Brillouin diversity index (Ĥ), which is more sensitive to the overall sample size Table 3. The results of the correlationthan the between Shannon the–Weaver number index, of Silphidae ranged and from the percentage0.752 to 1.991 content at the of individualexamined fractionssites. The in the soil parts. values of the Margalef’s diversity index, calculated on the basis of the natural logarithm (ln), ranged from 1.136 to 2.073 at the examined sites. Conversely, the dominance index ranged from 0.156 (site 2) to 0.628 (site 10). Fraction Sand Silt Clay (<) 3.3. Influence of(2–0.05 Soil Granulometric mm) Composition(0.05–0.002 on the Occurrence mm) of Silphidae The RP/RSweight * percentagep-Value of sand, silt RP/RS, and * clay fractionsp-Value in the RP/RSsoil at individual * p-Value sites was varied and statistically significant (χ2 = 171.05, DF = 24, p < 0.000001). By means of the Silphidae—total −0.430 0.143 0.648 0.017 0 1 correlation test we verified the presence of a relationship between the percentage content of individual fractionsSilphidae—species and the total number of harvested Silphidae, and whether there Oiceoptoma thoracicum L.was a relationship 0.463 between 0.111 the percentage 0.202 content of 0.508individual fractions−0.573 and the 0.041abun- Phosphuga atrata atrata L. dance of individual0.637 Silphidae0.019 species (Table−0.508 3). 0.077 −0.301 0.318 Silpha carinata Hbst. 0.200 0.512 −0.085 0.782 0.155 0.612 TableSilpha 3 obscura. The results obscura of theL. correlation between−0.479 the number 0.097 of Silphidae 0.494and the percentage 0.086 content of indiv 0.364idual fractions 0.222 in theSilpha soil parts tristis. Ill −0.035 0.910 0.491 0.088 −0.070 0.821 Thanatophilus rugosus L. −0.316 0.294 0.386 0.192 0.285 0.346 Thanatophilus sinuatus F. −0.771 0.002 0.485Fraction0.093 0.598 0.031 Nicrophorus humator Gleditsch 0.352Sand 0.238 0.076Silt 0.804 −0.488 0.091 Clay (<) Nicrophorus interruptus Steph. −0.011(2–0.05 0.971mm) 0.019(0.05–0.002 mm 0.950) −0.008 0.979 Nicrophorus investigator Zett. 0.108RP/RS * 0.725p-Value 0.418RP/RS * p 0.156-Value RP/RS−0.318 * p-Value 0.290 NicrophorusSilphidae sepultor—Charp.total −0.030−0.430 0.9210.143 0.1900.648 0.5350.017 0.1890 1 0.537 Nicrophorus vespillo L. −0.033Silphidae 0.915—species 0.213 0.485 0.138 0.653 NicrophorusOiceoptoma vespilloides thoracicumHbst. L. 0.5540.463 0.0500.111 0.0220.202 0.9430.508 −−0.5730.711 0.0410.006

*—dependingPhosphuga on the atrata distribution atrata L. of the examined feature,0.637 the Pearson0.019 linear correlation−0.508 (R P) or Spearman’s0.077 rank correlation−0.301 (RS) test0.318 were used for analysis.Silpha Boldcarinata font Hbst. indicates a statistically significant0.200 result0.512 (p < 0.05). −0.085 0.782 0.155 0.612 Silpha obscura obscura L. −0.479 0.097 0.494 0.086 0.364 0.222 Silpha tristis Ill A positive− correlation0.035 and0.910 a statistically0.491 significant0.088 relationship −0.070 were found0.821 between Thanatophilus rugosusthe L. total number−0.316 of collected 0.294 specimens 0.386 and the share0.192 of the mechanical0.285 fraction0.346 with a Thanatophilus sinuatusdiameter F. of 0.05–0.002−0.771 mm (silt0.002fraction): 0.485 RS = 0.6482220.093 (Figure 60.598a). For the mechanical0.031 fraction with a diameter of 2–0.05 mm (sand fraction) the correlation was negative, but sta- Appl. Sci. 2021, 11, 1017 8 of 13

Appl. Sci. 2021, 11, x FOR PEER REVIEW 9 of 14 tistically insignificant. Conversely, for the mechanical fraction with a diameter <0.002 mm (clay fraction), there was no relationship (no correlation; RS = 0).

a b

c d

e f

g

FigureFigure 6. 6. ScatterplotsScatterplots showing showing correlation correlation between: between: (i) percentage (i) percentage fraction fraction of silt of (0.05–0.002 silt (0.05–0.002 mm) mm)and numbers and numbers of Sil- of phidaeSilphidae (a); ((ii)a); percentage (ii) percentage fraction fraction of sand of sand (2–0.05 (2–0.05 mm) mm) and and numbers numbers of P. of atrataP. atrata atrata atrata (b),(b T.), T.sinuatus sinuatus (c),(c N.), N. vespilloides vespilloides (d();d ); percentagepercentage fraction fraction of of clay clay (<0.002 (<0.002 mm) mm) and and numbers numbers of of O.O. thoracicum thoracicum (e(),e), T.T. sinuatus sinuatus (f()f )and and N.N. vespilloides vespilloides (g(g).).

A statistically significant relationship between the number of collected Silphidae and the share of the mechanical fraction with a diameter of 2–0.05 mm (sand fraction) was demonstrated for three species. In the case of Phosphuga atrata atrata (Figure 6b) and Nicrophorus vespilloides (Figure 6d) the correlation was positive. A statistically significant Appl. Sci. 2021, 11, 1017 9 of 13

A statistically significant relationship between the number of collected Silphidae and the share of the mechanical fraction with a diameter of 2–0.05 mm (sand fraction) was demonstrated for three species. In the case of Phosphuga atrata atrata (Figure6b) and Nicrophorus vespilloides (Figure6d) the correlation was positive. A statistically significant correlation was also found for Thanatophilus sinuatus (Figure4c), however the correlation was negative. With regard to the mechanical fraction with a diameter of <0.002 mm (clay fraction), a statistically significant relationship was observed for Oiceoptoma thoracicum (Figure6e) and N. vespilloides (Figure6g), for which the correlation was negative. However, for T. sinuatus (Figure6f), a positive correlation was found in this case.

4. Discussion The soil preferences of Silphidae were previously investigated by i.e., Novák [22,23], Trumbo and Bloch [24], Bishop et al. [25], Bedick et al. [26]. The studies of Bishop et al. [25], Jakubec and R ˚užiˇcka[27] and Hoermann et al. [28], also present the relationships for the Silphinae subfamily (the first two papers mentioned) in addition to statistical analysis. Nevertheless, with respect to Silphidae (especially Silphinae), some environmental factors, especially those related to the soil environment, still remain unrecognized. The soil granulometric composition is an important physical parameter of mineral soils. It determines almost all physical, chemical, and biological properties of soils. In line with our expectations, the study showed that the soil grain size composition was an important factor influencing the settlement of Silphidae. Taking into account the influence of the soil particle size distribution on the Silphidae assemblages in general, it was shown that only one statistically significant factor influenced the occurrence of beetles. It was observed that with the percentage increase of the silt fraction, the total number of specimens increased. The sites with the highest percentage of this mechanical fraction (>70%; site 1, 2, 3, 10, and 13) were characterized by a higher number of collected Silphidae, although the quantitative structure of these areas was dominated by the presence of two species: T. sinuatus and N. vespilloides. Moreover, the studies by Hoermann et al. [28] proved that the Simpson dominance coefficient showed an upward trend along with a higher silt content at the examined sites. The relationship between the percentage of sand fraction and the total abundance of Silphidae was negatively correlated, although statistically insignificant. However, other studies indicated that this fraction had a significant impact on the hunting ability of carrion beetles [5,25]. Conversely, there was no correlation between the number of the carrion beetles and the percentage of the clay fraction (RS = 0). The obtained result is partially consistent with studies by Hoermann et al. [28], where this fraction was insignificant as the only predictive variable. Despite differences in statistical interpretation, both results generally suggest no relationship between the content of this mechanical fraction and the abundance of Silphidae. In terms of representatives of the genus Nicrophorus, the results obtained by us were consistent with studies by other authors on one species—N. vespilloides. Moreover, it was the only Nicrophorus species that showed a statistically significant relationship between the mechanical fraction of the soil and the abundance. The abundance of this species increased in the sites with a higher percentage of sand (sites 3, 4, 5, and 6). Hoermann et al. [28] showed this relationship not only for N. vespilloides, but also for Nicrophorus humator. In our study, this tendency was observed at sites where a simultaneous decrease in the content of the clay fraction was noted, with which the number of N. vespilloides was negatively correlated and statistically significant. We also found a positive correlation with N. humator, but the correlation was insignificant. The impact of the content of sand fractions on the occurrence of beetles varies (is posi- tively or negatively correlated, statistically significant or insignificant) for different species. Lomolino et al. [5] showed a relationship between an increase in the catchability of Nicropho- Appl. Sci. 2021, 11, 1017 10 of 13

rus americanus and an increase in sand fractions, with a simultaneous decrease in the content of silt and clay fractions, which is partially consistent with our results for N. vespilloides. Conversely, the occurrence of Nicrophorus orbicollis and N. marginatus was not statistically related to the sand fraction. In contrast, for N. marginatus and Nicrophorus tomentosus Bishop et al. [25] showed the dependence of the abundance of the mentioned species in relation to the sand fraction, which was positively correlated. For the remaining representatives of this genus, the analysis of the percentage depen- dence of the individual soil mechanical fractions (silt and clay fractions) and catchability and the number of individuals showed a different correlation (positive or negative) but was statistically insignificant. It is worth noting, however, that for all recorded representatives of this genus (6 species), despite the statistical insignificance, the correlation between the number of beetles and the content of silt fractions was positive. The preference of such surfaces may be related to the properties of this fraction, which increases water infiltration, especially in light sandy soils. The abundance of O. thoracicum showed an upward trend in the sites where a decrease in the percentage of the clay fraction was observed. It was also observed that the abundance of this species increased in sampled areas with more abundant sand fractions. Although this correlation was not statistically significant, the same tendency was observed for the previously mentioned N. vespilloides. Despite taxonomic and ecological diversity, they are considered forest species and prefer similar habitats [29]. Both mentioned species of Silphidae were indicated in the study conducted by Jakubec and R ˚užiˇcka[27]; however, due to the unrepresentative number of the collected specimens, they were not included in the statistical analysis. The same authors indicated that P. atrata atrata, a species which, also due to its low number, was not analyzed (n = 1). On the other hand, in our study, P. atrata atrata occurred in greater numbers (n = 470), much more in areas where the percentage of sand fraction was within the range of 19–56% (mean: 34.6% ± 14.11), compared to areas with sand fractions in the range of 10–19% (average: 15.0% ± 2.94). Another representative of Silphinae showing significant correlations between the num- ber of collected specimens and the percentage of soil mechanical fractions was T. sinuatus. It was the most abundant species of all the Silphidae collected (n = 3599). Its number was negatively correlated with the percentage of sand fraction, and positively with the clay fraction. The number of T. sinuatus, exceeding 100 individuals, was observed in sites with a lower percentage of sand fraction (average sand fraction content in sites with more than 100 individuals—15.62% ± 3.02, compared to sites with less than 100 individuals—33.6% ± 15.59) and higher percentage content of the clay fraction (the average content of the clay fraction at sites with more than 100 individuals—17.0% ± 6.90, compared to sites with less than 100 individuals—6.4% ± 5.12). In the study by Jakubec and R ˚užiˇcka[27], it was also the most numerous species, showing a statistically significant correlation between the number of individuals caught and the soil type. The authors showed that T. sinuatus was caught on alluvial more often than in black soils. Studies of entomofauna inhabiting sandy sites (including dunes) showed a very large number of this species, which is often dominant [30–32], which contrasts with our results. Conversely, Wolender and Zych [33] did not show the presence of this species in their observations of coleopterofauna of beaches and dunes. Studies on the presence of other representatives of the genus Thanatophilus showed that T. lapponicus was present almost exclusively in pastures with sandy soils and avoided sandy farmlands. Contrasting results have been reported for T. truncatus, which, as a generalist species, appears to be less susceptible to the effects of agriculture [25]. Furthermore, in Lingafelter’s study [34], both of these species were more numerous on open, sandy prairies, avoiding forests and non-sandy sites. It can be assumed that the greater presence of T. sinuatus in arable fields is related to the physical properties of the outer part of the soil, which due to agricultural use does not form a compact and uniform layer, allowing insects to bury themselves in periods of Appl. Sci. 2021, 11, 1017 11 of 13

reduced activity [25] or lay eggs near carrion [1]. Both males and females are polygamous and can mate multiple times in a single day [35]. Due to the high reproductive activity of this West Palearctic species (iteropathic species; three generations per year) [17], the existence of certain relationships related to the occurrence of this species and the soil structure should be expected.

5. Conclusions 1. Soil granulometric composition is an important parameter of the soils of the habitat and may determining their colonization by the carrion beetles (Coleoptera: Silphidae). 2. A positive correlation and a statistically significant relationship were found between the total number of Silphidae and the share of the mechanical fraction of soil with a diameter of 0.05–0.002 mm (silt fraction). 3. In the case of representatives of Nicrophorinae, the only species showing a statistically significant relationship between the abundance and the proportion of mechanical fractions was N. vespilloides. 4. Among the representatives of Silphinae, a statistically significant relationship between the abundance and the content of soil mechanical fractions occurred in the case of O. thoracicum. P. atrata atrata, and T. sinuatus.

Supplementary Materials: The following are available online at https://www.mdpi.com/2076-3 417/11/3/1017/s1. Table S1: Species composition, abundance and dominant relations of Silphidae caught at individual sites, Figure S1: Dominance relations of Silphidae caught on each study sites. Data from two-year studies were averaged. Dominance structure was described according to the scale: ED—eudominants (above 10.0%), D—dominants (5.1–10.0%), SD—subdominants (2.1–5.0%), R—recedents (1.1–2.0%) and SR—subrecedents (below 1.0%) [19]. Author Contributions: Conceptualization, K.K. and Z.W.C.; methodology, K.K. and M.S.; soft- ware, K.K.; validation, K.K., Z.W.C., and M.S.; formal analysis, K.K., Z.W.C., and M.S.; investiga- tion, K.K. and M.S.; resources, K.K.; data curation, K.K.; writing—original draft preparation, K.K.; writing—review and editing, Z.W.C.; visualization, K.K.; supervision, Z.W.C.; project administration, Z.W.C.; funding acquisition, Z.W.C. All authors have read and agreed to the published version of the manuscript. Funding: The project is financed by the program of the Minister of Science and Higher Education named “Regional Initiative of Excellence” in the years 2019–2022, project number 026/RID/2018/19. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Department of Agroecology and Forest Utilization, College of Natural Sciences, University of Rzeszów. Conflicts of Interest: The authors declare no conflict of interest.

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