The importance of dung beetles and arthropod communities ... · dung pat and arthropod characteristics including pat wet weight, dry weight, moisture content, organic matter content,

Submitted 20 March 2018Accepted 22 June 2018Published 19 July 2018

Corresponding authorJonathan G Lundgrenjglentomologygmailcom

Academic editorNigel Andrew

Additional Information andDeclarations can be found onpage 15

DOI 107717peerj5220

Copyright2018 Pecenka and Lundgren

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

The importance of dung beetles andarthropod communities on degradationof cattle dung pats in eastern SouthDakotaJacob R Pecenka12 and Jonathan G Lundgren2

1Natural Resource Management Department South Dakota State University Brookings SDUnited States of America

2 Ecdysis Foundation Estelline SD United States of America

ABSTRACTBackground Dung accumulation in rangelands can suppress plant growth foulpastures and increase pest pressure Here we describe the arthropod community ofdung in eastern South Dakota and quantify their contributions to dung degradationusing an exclusion cage designMethods Various arthropod community and degradation characteristics were mea-sured in caged and uncaged dung pats over time in early and late summerResults A total of 86969 specimens were collected across 109 morphospecies (13orders) of arthropods and cages effectively reduced arthropod abundance speciesrichness and diversity Uncaged dung pats degraded significantly faster than the cagedpats with the largest difference occurring within 2 d of pat deposition Dung organicmatter was degraded more slowly (by 33ndash38 d) in the caged pats than where insectshad free access to the pats Although dung beetles only represented 15ndash3 of totalarthropod abundance theywere significantly correlated tomore abundant and complextotal arthropod communitiesDiscussion A diverse community contributes to dung degradation in rangelands andtheir early colonization is key to maximizing this ecosystem service

Subjects Agricultural Science Animal Behavior Biodiversity Ecosystem Science EntomologyKeywords Dung arthropod community Dung colonization Dung pat decomposition Nutrientcycling

INTRODUCTIONWhen cattle excrete dung onto the soil surface the failure of the pats to break down canchallenge the productivity of grazing on rangelands (Fincher 1981) When cattle consumeforage any nutrients not digested are returned to the system in the form of dung and urine(Haynes amp Williams 1993Wu amp Sun 2010) The undigested plant material that comprisesdung is deposited on the soil surface smothering plant growth in that area (Holter 2016MacLusky 1960) Pasture fouling through continuous dung deposition that fails to degradequickly can represent a substantial problem to ranchers if left unmanaged When a dungpat is deposited on a pasture all of the available forage underneath and up to a 5 mradius around the pat is unused by grazing cattle until the pat is incorporated into the soil

How to cite this article Pecenka and Lundgren (2018) The importance of dung beetles and arthropod communities on degradation ofcattle dung pats in eastern South Dakota PeerJ 6e5220 DOI 107717peerj5220

(Weeda 1967) Dung loses 22 (but up to 80) of its nitrogen (N) to volatilization within60 d of deposition (Nichols et al 2008 Weeda 1967) Other important nutrients such asphosphorus (P) and potassium (K) are present in dung pats in much smaller quantities andcan be lost to leaching and runoff when left on the soil surface (Gillard 1967 Nichols et al2008 Petersen Lucas amp Woodhouse 1956) Volatilization and reductions of these elementsdecreases the nutrient availability to the plant community resulting in lower quantity andquality of forage for future cattle grazing (Aarons et al 2009 Bang et al 2005)

A variety of factors affect how quickly dung is incorporated into the soil Reports ofdung degradation rates vary from 50ndash65 d over the season (Holter 1979) 57ndash78 d in latespring to 88ndash111 d in late summer (Lee amp Wall 2006) and up to 3 y in cattle grazingsystems with high insecticide use (Anderson Merritt amp Loomis 1984 Strong 1992) Thisvariability is due to factors that include weather (Holter 1979) seasonality (Lee amp Wall2006) insecticide use (Suarez et al 2003) and the nutritional quality of the dung itself(Cook Dadour amp Ali 1996) Degradation of dung pats is facilitated by arthropods thataccelerate the incorporation of the dung pat organic matter into the soil and improvesoilrsquos aeration and water holding capacity (Macqueen amp Beirne 1975) Dung often supportsdozens or even hundreds of arthropod species (Blume 1985 Merritt amp Anderson 1977Valiela 1969)

Arthropods that colonize dung pats can be categorized into different functional guildsthat each contribute to the eventual incorporation of the dung into the soil One ofthe first studies that considered dung community function was Mohr (1943) whichprompted other studies that documented arthropod succession in a dung pat and theirvarying niches within the micro-habitat (Cervenka amp Moon 1991 Koskela amp Hanski 1977Sanders amp Dobson 1966) These studies are accompanied by more recent explorationsof the importance of dung beetles (Scarabaeidae) and the multiple ecosystem servicesthat they provide (Beynon et al 2012 Manning et al 2016 Nichols et al 2008) One ofthese ecosystem services is dung beetlesrsquo ability to increase the productivity of rangelandecosystems (Bang et al 2005 Penttila et al 2013) Increased rangeland productivity isachieved by bioturbation and burial of dung that results in capturing ephemeral nutrientsfor surrounding forage plants up to 127 cm away from the dung pat (Bornemissza 1970Macqueen amp Beirne 1975 Yamada et al 2007) A second important ecosystem service isthe suppression of dung inhabiting pests to grazing cattle (Fincher 1981) By removingnutritional resources and habitat dung beetles reduce pest maggot abundance (Doube1990 Nichols et al 2008) Suppressing these pests is accelerated when natural enemiessuch as predatory staphylinid or hister beetles and parasitoid wasps colonize the dungpat (Cervenka amp Moon 1991) These ecosystem services provided by dung beetles (as wellas other members of the dung arthropod community) have an economic value to theranching operation (Beynon Wainwright amp Christie 2015) but most of the numbers usedto generate these values are at least 37 years old (Beynon et al 2012 Fincher 1981 Losey ampVaughan 2006)

The goal of our study was to document the dung insect community in eastern SouthDakota and determine dung degradation rates over time in the presence and absenceof this community Cages like those employed here help to isolate the contribution of

Pecenka and Lundgren (2018) PeerJ DOI 107717peerj5220 219

the majority of the arthropod community to dung pat degradation (Lee amp Wall 2006Tixier Lumaret amp Sullivan 2015) Here we pair cages with a comprehensive descriptionof invertebrate communities within the dung both early and late in the summer tounderstand how elements of this community affect degradation over the season There are912 million ha of rangeland in South Dakota (USDA-NASS) and this region representsan important transition zone between the mid and tall-grass prairie biomes (NASS 2016)Dung-inhabiting Coleoptera from South Dakota were described nearly 50 years ago(Kessler amp Balsbaugh 1972 McDaniel Boddicker amp Balsbaugh 1971) but these studies didnot correlate these insects to dung pat degradation and land use patterns have changeddramatically toward annual cropland over this period of time (Johnston 2014 Wright ampWimberly 2012) Identifying the impact of the dung arthropod community on degradationwill provide ranchers a greater understanding of the benefits of conserving this poorlyunderstood community We hypothesize that caging pats will reduce insect colonizationof the dung and impede pat degradation rates

MATERIALS AND METHODSStudy siteThis study was conducted on a ranch in eastern South Dakota US at 44758 minus96538 inthe summer of 2016 The study site was at an altitude of 559 m in an area with an averageannual rainfall of 684 mm and an average summer temperature of 198 C The 130 hapasturewas composed ofmixed grasses consistingmostly of Schizachyrium scoparium (littlebluestem) Andropogon gerardii (big bluestem) and Spartina pectinata (prairie cordgrass)with predominantly silty clay and silty clay loam soil types (USDA-NRCS 2016) Thegrazing season prior to and during the experiment had a 130-steer herd made up ofAngus Belted Galloway and Irish Black breeds that was moved among small 041ndash121ha paddocks approximately every 24 h Cattle were excluded from the experimental siteduring the observation periods No insecticide or nematicide treatments had been used oncattle on this ranching operation in more than 10 y

Dung degradation measurementsDung (lt2 h old 90 kg collected twice) was collected from the pasture on 04062016 and05062016 before 1000 Fresh dung pats were homogenized and stored in bags atminus25 Cfor 72 h to ensure all arthropods had been killed Dung was removed from the freezercompletely thawed and homogenized prior to use in the experiment Aliquots of the dung(1000 plusmn 10 g) were weighed individually bagged and stored for 24 h before placing themin the field Each bag of weighed dung became a lsquolsquosentinel patrsquorsquo to represent a dung patdeposited by grazing cattle Observation sites (n= 84) were placed in the pasture so siteswere at least 5 m apart At each site a sentinel pat was placed on top of mesh with 25 cmsquare holes to allow for ease of pat removal Each site was randomly assigned to one ofthree treatments In the first treatment (inclusion n= 36) dung pats were left completelyexposed with no covering In the second treatment (exclusion n= 36) the pats weresurrounded by a PVC cylinder (25 cm diam 25 cm tall) buried at least 12 cm into theground to reduce ground colonization of the pat The tops of these cylinders were covered


in fine mesh screen (lt1 mm opening) and secured with a plastic tie The final controltreatment (sham cage n= 12) used the same cylinder design as the exclusion treatmentbut with three 10 times 10 cm holes cut on the sides to allow arthropods to travel into thecylinder A wire top was used to cover these sham cylinders that had 3 cm openings Thisthird treatment was added to test whether the exclusion cage had direct effects on dungdegradation rates

To determine degradation rates pats from the three treatments were weighed over timeThe entire experiment was repeated twice over the season once beginning on 10-Juneand once on 28-July Randomly selected pats (Inclusion [six pats] Exclusion cage [six]and Sham cage [two] on each time point) were removed 2 4 7 14 28 and 42 d after thesentinel pats were placed At the time of removal the pat was collected in a plastic bagsealed and taken to the laboratory Each pat was weighed while still fresh and after dryingto constant weight (over 7ndash10 d) A 10-gram sample of this dried pat was ground to afine powder and baked at 500 C for 1 h the remaining sample was then re-weighed todetermine ashmineral content of the sample From this value the ash-free organic mattercontent (AFOM) of the pat was calculated

Arthropod collection and dung pat analysisThe pat was weighed and placed in a Berlese funnel system for 7 d to extract arthropodsliving in the dung pat The top of the extraction funnel sealed with the top board of thisextraction system eliminating the ability of winged arthropods to escape The arthropodswere identified under a microscope and then weighed to calculate arthropod biomassTo help characterize this diverse arthropod community each specimen was identifiedto the lowest taxonomic level possible Specimens were identified to at least the familylevel using Triplehorn amp Johnson (2005) and scarabid beetles were identified to speciesby Ratcliffe amp Paulsen (2008) Within these families each specimen was assigned to amorphospecies and functional guild depending on their feeding ecology The non-pest coprophagous community was divided into macro-coprophages (gt1 mm longScarabaeidae Hydrophilidae) andmicro-coprophages (lt1mm long Acarina CollembolaPtiliidae)

Data analysisAll statistics were conducted using Systat 13 (SYSTAT Software Inc Point RichmondCA) Two-way ANOVAs were used to investigate how dung pat age and cages affecteddung pat and arthropod characteristics including pat wet weight dry weight moisturecontent organic matter content and arthropod biomass abundance species richness(number of morphospecies found) species diversity (Shannon H) and abundance offamily Scarabaeidae To avoid possible pseudoreplication and sampling bias separateanalyses were conducted on data collected early and late in the season ANOVAs wereused to compare the abundances of coprophages predators parasitoids herbivores andmaggots collected per pat early and late in the season Linear regressions were generated tocompare the number of dung beetles to dung pat organic matter total arthropod biomassarthropod abundance species richness species diversity andmicro-coprophage abundance


(pooled across pat ages and earlylate season observations) Many cross comparisons ofdifferent community characteristics and response variables can lead to false positives ortype I errors in our analyses Prior to running any statistical tests we always investigatethe patterns in the data looking for biologically meaningful trends This helps to reducethe likelihood of type I errors and increase the relevance of our results

RESULTSDung arthropod communityA total of 109 morphospecies (86969 arthropod specimens) were collected from dung patsrepresenting 13 orders (Acarina Araneae Coleoptera Collembola Diptera HemipteraHymenoptera Isopoda Julida Lepidoptera Lithobiomorpha Pseudoscorpiones andThysanoptera) There were 51768 plusmn 3098 (mean plusmn SEM) larval and adult specimenscollected (22802 plusmn 4605 mg of arthropods) represented by 1332 plusmn 049 morphospeciesper dung pat Larval communities included only three orders Diptera (six morphospecies)Coleoptera (17 morphospecies) and Lepidoptera (one morphospecies) Orders with themost abundant specimens were Acarina (n= 35534) Coleoptera (adult n= 22689 larvaen= 6057) Collembola (n= 9114) Diptera (adult n= 609 larvae n= 8870) Lepidoptera(adult n= 8 larvae n= 2034) and Hymenoptera (n= 1141) Four families of Coleopterawere well represented (they comprised 26 of all specimens collected) Staphylinidae(n= 8140) Ptiliidae (n= 9247) Hydrophilidae (n= 3576) Scarabaeidae (n= 1624)were represented by 14 one 12 and 13 morphospecies from these families respectivelyTrophically these specimens were categorized as coprophagous (37 morphospecies60564 specimens) predators (38 morphospecies 15047 specimens) herbivores (18morphospecies 2037 specimens) or parasitoids (10 morphospecies 539 specimens) Theremaining specimens are regarded as coprophagous maggots (6 morphospecies 8870specimens) consisting of Diptera larvae

Arthropods were collected early and late in the summer Arthropod abundancesin the early season were 48563 plusmn 4218 (40765 total) specimens from 1291 plusmn 071morphospecies per pat 54973plusmn 4536 (46269 total) arthropods representing 1373plusmn 067morphospecies per pat were collected later in the summer Arthropod biomass per pat was35793plusmn 4098 mg in the early season and 15272plusmn7240 mg in the late season Functionalgroup populations changed between the two sampling periods Coprophage abundancesignificantly (F = 508 df = 1166 P = 0026) increased 26 (25837 to 34639) predatorabundance significantly (F = 911 df = 1166 P = 0003) increased 40 (5661 to 9386)parasitoid abundance significantly (F = 2436 df = 1166 P lt 0001) decreased by 78(442 to 97) herbivore abundance significantly (F = 789 df = 1166 P = 0012) decreasedby 53 (1389 to 648) and maggots significantly (F = 1225 df = 1166 P = 0001)decreased by 79 (7371 to 1499) from early to late summer Dung beetles represented3 and 15 of total arthropod abundance in early and late season respectively

Sham cage effectThe sham cages had similar arthropod communities and dung characteristics with the nocage treatment in 16 of the 18 ANOVAs of different dung arthropod community groups


and dung degradation metrics Only early season arthropod abundance and late seasondung pat wet weight were significantly different between cage treatments but these trendswere not consistent in both early and late seasons The general lack of differences betweenthe sham cage and no cage treatments indicates that the cage had little direct effect onarthropod communities and dung characteristics and justifies our focus on cageno cagecomparisons for the remainder of this section

Treatment and time effect on dung communityDung pats in the pasture had different arthropod communities when pats were caged andas the dung pat aged Cages and time had a significant effect on arthropod biomass in theearly and late seasons (Fig 1) Arthropod biomass inside the cages was 10 of the biomassfound in the uncaged pats early in the season and caged pats had 13 of the biomassof the uncaged later in the summer The biomass and abundances (Fig 2) of arthropodswere significantly greater on younger pats (2 4 and 7 d old) versus older pats (14 28 42 dold) both early and late in the season Specifically the biomasses declined by 72 and 83between the 7th and 14th days in early and late season respectively After 14 d arthropodbiomass did not significantly change through 42 d Caged dung pats only averaged 52and 57 of the arthropod specimens that were found in the inclusion dung pats in earlyand late seasons respectively

Cages did not completely exclude the insect community but it did reduce the arthropodspecies richness and diversity The richness of arthropod species found in the dung pats wassignificantly affected by cages and time in the early season (exclusion F = 10286 df = 160P lt 0001 time F = 508 df = 560 P lt 0001 interaction F = 671 df = 560P lt 0001) and in the late season (exclusion F = 6649 df = 160 P lt 0001 timeF = 2644 df = 560 P lt 0001 interaction F = 670 df = 560 P lt 0001) The meannumber of species in the caged dung pats were 46 and 62 of the number in the uncagedpats for the early and late season respectively Cages and time had a significant effect onarthropod diversity (ShannonH) in the early season (cage F = 3424 df = 160 P lt 0001time F = 1071 df = 560 P lt 0001 interaction F = 503 df = 560 P = 0001) butonly time had a significant effect in the late (cage F = 040 df = 160 P = 0528 timeF = 5019 df = 560 P lt 0001 interaction F = 553 df = 560 P lt 0001) season Therewere significantly more maggots (F = 4737 df = 266 P lt 0001) in the caged than theuncaged pats Dung beetle abundance was significantly reduced by the arthropod exclusionIn the early season cages and time had a significant effect on dung beetle abundance (cageF = 11155 df = 160 P lt 0001 time F = 1730 df = 560 P lt 0001 interactionF = 1795 df = 560 P lt 0001) Likewise in the late season cages and time had asignificant effect on dung beetle abundance (cage F = 10501 df = 160 P lt 0001 timeF = 2385 df = 560 P lt 0001 interaction F = 2385 df = 560 P lt 0001)

The effects of arthropod reduction and time on dung degradationCages and time had significant effects on dung pat wet weight in both the early and lateseason (Table 1) Dung from which many insects were excluded had an average of 2610


Figure 1 Arthropod dry weight biomass (meanplusmn SEM) per cattle dung pat (n= 6) over the age of thepat lsquolsquoExclusionrsquorsquo refers to caged pats lsquolsquoInclusionrsquorsquo refers to uncaged pats Arthropods were excluded fromhalf of the pats (n = 6 pats per treatment per age) using cages Pats were examined beginning in June (A)and in late July (B) Asterisks above the bars indicate significantly different arthropod biomasses in thecaged and uncaged pats for that specific sample age (α= 005)

Full-size DOI 107717peerj5220fig-1

and 2193 lower wet weights and dry weights (in the early and late seasons) (Table 1)than when arthropods were allowed access to the pats Pats experienced a 283plusmn 194 wetweight loss during the first 2 d and 7970plusmn 128 weight loss by day 42 (Table 1) Moistureof dung pats was significantly correlated with arthropod abundance in early (F170= 2359


Figure 2 Arthropod abundance (meanplusmn SEM) per cattle dung pat (n = 6) over the age of the patlsquolsquoExclusionrsquorsquo refers to caged pats lsquolsquoInclusionrsquorsquo refers to uncaged pats Arthropods were excluded from halfof the pats (n = 6 pats per treatment per age) using cages Pats were examined beginning in June (A) andin late July (B) Asterisks above the bars indicate significantly different arthropod abundances in the cagedand uncaged pats for that specific sample age (α= 005)


P lt 0001) and late (F170= 999 P = 0002) seasons After drying the uncaged dung patscontained 2545 and 2510 less weight than the caged dung pats

The ash-free organic matter (AFOM) percentage of the dried dung patsrsquo remainingweight was significantly affected by exclusion cages and time in the early and late seasons(Table 1) Throughout the season the uncaged dung pats had significantly less AFOM


Table 1 The effects of age in days since deposition (0ndash42 days) on of the weight and ash-free oganic matter of dung pats These characteristicswere studied over time when insects were allowed access to (inclusion) or were excluded from the pats using cages Communities were sampled earlyin the season and late in the season and are presented distinctly Data presented represents the meanplusmn SEM Capital letters represent differencesover time and lower case letters represent differences between treatments (α= 005)

Days Wet weight of pat (g) Dry weight of pat (g)

Exclusion cage Uncaged Exclusion cage Uncaged

2 77278plusmn 2434 Aa 58511plusmn 3012 Ab 19305plusmn 418 Aa 14738plusmn 1210 AbEarly season

4 69725plusmn 1558 Ba 52128plusmn 2921 ABb 14491plusmn 597 Ba 10314plusmn 714 BCb7 64855plusmn 2470 Ba 49795plusmn 1877 Bb 1355plusmn 276 BCa 11830plusmn 668 BCb14 35996plusmn 1728 Ca 26194plusmn 2836 Cb 15693plusmn 350 Ba 10387plusmn 1077 BCb28 29015plusmn 1859 Da 21504plusmn 989 Cb 13575plusmn 324 BCa 9955plusmn 796 BDa42 19322plusmn 1592 Ea 13388plusmn 540 Db 11541plusmn 204 Da 8419plusmn 341 Da

exclusion F160= 10421 P lt 0001time F560 = 20796 P lt 0001

interaction F560= 331 P = 0010


interaction F560= 886 P lt 00012 82921plusmn 1404 Aa 70813plusmn 1342 Ab 30164plusmn 562 Aa 23764plusmn 286 Ab

Late season4 70210plusmn 957 Ba 53584plusmn 1021 Bb 21766plusmn 664 Ba 18675plusmn 155 Bb7 74168plusmn 1095 Ba 63058plusmn 710 Cb 22030plusmn 223 Ba 18711plusmn 211 Bb14 71234plusmn 1314 Ba 60570plusmn 985 Cb 22727plusmn 699 Ba 16989plusmn 389 Cb28 44228plusmn 1097 Ca 27427plusmn 1031 Db 19133plusmn 280 Ca 11569plusmn 409 Db42 29396plusmn 947 Da 21938plusmn 855 Eb 18130plusmn 379 Ca 11721plusmn 452 Db


interaction F560= 568 P lt 0001



Days Ash free organic matter weight of dried dung (g) Ash free organic matter ( of dry weight)



4 12512plusmn 606 Ba 8083plusmn 527 Bb 8627plusmn 149 ABa 7852plusmn 112 Ab7 11467plusmn 190 BCa 9232plusmn 541 Bb 8465plusmn 060 ABa 7801plusmn 053 ABb14 13328plusmn 311 Ba 7951plusmn 808 BCb 8493plusmn 069 ABa 7660plusmn 065 Bb28 11451plusmn 307 BCa 7413plusmn 563 BCb 8433plusmn 027 Ba 7461plusmn 050 Ca42 9257plusmn 172 Da 5867plusmn 232 Db 8021plusmn 053 Ca 6970plusmn 023 Db




interaction F560= 160 P = 01752 26733plusmn 644 Aa 20423plusmn 392 Ab 8858plusmn 059 Aa 8591plusmn 082 Ab

Late season4 19059plusmn 555 Ba 15849plusmn 150 Bb 8759plusmn 053 ABa 8487plusmn 080 ABb7 19265plusmn 183 Ba 15861plusmn 249 Bb 8717plusmn 046 ABCa 8475plusmn 096 ABa14 19765plusmn 651 Ba 14199plusmn 291 Cb 8695plusmn 060 BCa 8361plusmn 085 Bb28 16424plusmn 255 Ca 9455plusmn 317 Db 8584plusmn 042 Ca 8176plusmn 089 Cb42 15566plusmn 285 Ca 9363plusmn 361 Db 8588plusmn 038 Ca 7988plusmn 047 Db






than the caged pats Initially 9026 of dried dung pats were AFOM by weight and bythe 42nd day it decreased to 69ndash80 for uncaged pats and 80ndash86 for caged pats Earlyseason uncaged dung pats averaged 68 less AFOM than caged pats and late season patsfollowed a similar trend with 314 less AFOM in the uncaged compared to the caged patsEarly and late season AFOM weight was also significantly affected by exclusion cages andtime (Table 1) and the loss of AFOM weight was different between treatments (Fig 3)Early season dung pats with arthropods are estimated to completely degrade before 71 dand this increases to 104 d when arthropods are excluded from the pats with cages Lateseason dung pats achieve complete breakdown at a faster rate with estimates of 61 d and100 d in uncaged and caged pats respectively

Effect of dung beetles on arthropod communityAlthough they represented 15ndash3 of the arthropod community recovered dung beetleabundance diversity and richness were always positively correlated with arthropodcommunity characteristics (Table 2) The abundance of dung beetles was significantly andpositively correlated with total arthropod biomass arthropod abundance total speciesrichness and abundance of the micro-coprophage community in both the early andlate seasons Dung beetle species richness and diversity was correlated to an increase inabundance of the entire dung arthropod community in both early and late seasons (Table 2)(Fig 4)

DISCUSSIONDung degraded more quickly when all arthropods were allowed access to the dung patDung pat wet weight dry weight moisture percentage and AFOM all decreased overtime during the 42-d observation period (Table 1 Fig 3) The degradation characteristicsalso show that uncaged pats degraded faster than the caged ones Ash-free organic matter(AFOM) has been proposed as the most accurate measure of dung pat degradation(Holter 1979) When arthropods were allowed to colonize dung pats AFOM was reducedsubstantially within the first 2 d (Fig 3) This quicker degradation may be explained byearly colonization of the pat by relatively large arthropods Dung beetles are some of thelargest dung arthropods and the amount of dung they consume and remove from thepat for oviposition is disproportionate compared to their abundance in the dung pats(McDaniel Boddicker amp Balsbaugh 1971) After this first 2 d the pats degraded at similarrates in both the caged and uncaged pats When insects were allowed access to the pats thepats had 32 of the original AFOM after 42 d caged pats had 55 of the AFOM at the endof the observation period Extrapolations of the data show that insects shorten the lives ofpats (ie complete AFOM removal) by an estimated 33 d in the early season and by 38d later in the season These observations are comparable to dung degradation estimatesmade in similar studies (Lee amp Wall 2006 Tixier Lumaret amp Sullivan 2015) Often theseexamples only exclude arthropods for short periods of time or focus on the collection ofa single arthropod group limiting the scale and scope of the observations made Resultsshow that early dung pat degradation sets the tone for the remainder of the dung patrsquos timeon the soil surface (ie the slopes of the regressions presented in Fig 3) This suggests that


Figure 3 Degradation rate of organic matter content (meanplusmn SEM) in cattle dung pats lsquolsquoExclusionrsquorsquorefers to caged pats lsquolsquoInclusionrsquorsquo refers to uncaged pats Dung pats were dried to 0 moisture and burnedin furnace to remove all organic matter allowing calculation of ash-free organic matter content (AFOM)AFOM content was calculated in dung pats beginning in June (A) and late July (B) Half of pats hadarthropods excluded (n= 6 pats per treatment per dung age) compared to allowing uninhibited arthropodcolonization



Table 2 Relationships of dung beetle abundance richness and diversity to the arthropod community characteristics when complete insectcommunities were allowed access to dung pats Communities were sampled early in the season and late in the season and are presented distinctlyData presented represents the meanplusmn SEM Statistical presentation are the result of linear regressions and α= 005

Dung beetle

Characteristic Abundance Richness Diversity

Early season Arthropod biomass (mg) F135= 4764 P lt 0001 F135= 7446 P lt 0001 F135= 5942 P lt 0001Arthropod abundance F135= 4484 P lt 0001 F135= 1507 P lt 0001 F135= 1073 P = 0001Species richness F135= 4253 P lt 0001 F135= 7446 P lt 0001 F135= 1631 P lt 0001Micro-coprophage abundance F135= 5280 P lt 0001 F135= 1969 P lt 0001 F135= 1516 P lt 0001

Late season Arthropod biomass (mg) F134= 7080 P lt 0001 F134= 6394 P lt 0001 F134= 6120 P lt 0001Arthropod abundance F134= 2723 P lt 0001 F134= 3000 P lt 0001 F134= 2754 P lt 0001Species richness F134= 4295 P lt 0001 F134= 6394 P lt 0001 F134= 8197 P lt 0001Micro-coprophage richness F134= 2506 P lt 0001 F134= 2865 P lt 0001 F134= 2831 P lt 0001

even a short period of exclusion could have implications for the degradation of a dungpat Disruptions to early arthropod colonization can have long-term implications to theefficient recycling of dung pats

With few exceptions the cages effectively reduced both the diversity and abundanceof arthropods in cattle dung pats The arthropods found in caged dung pats were thoseexisting in the surrounding soil and those species that were small enough to fit through theexclusion screen (eg flies laid their eggs on the screen and neonate larvae fell through ontothe dung pat) There was significantly higher arthropod abundance and biomass foundin the uncaged pats that were younger than 7 d old (Figs 1 and 2) These significantlyhigher numbers of early colonizers corroborate previous work that showed that the highestdensities of invertebrates occur between 2 and 5 d post-deposition (Kessler amp Balsbaugh1972 Lee amp Wall 2006) Most of the arthropods found in the caged dung pats were smallhydrophilid beetles ptiliid beetles mites and Collembola which collectively are describedas lsquolsquomicro-coprophagesrsquorsquo This group frequently colonized both caged and uncaged patsdue to their small size and presence in the soil prior to cage placement Another groupfound in both treatments was dipteran larvae indeed we found more maggots in the cagedpats than the uncaged pats Overall there was a significant and substantial reduction in thebiomass abundance and diversity of most the dung arthropods in the cages

Arthropod community complexity and abundance diminished as the pat aged past 7days Many of the early dung colonizers (flies and coprophagous beetles) consume smallparticles found in the liquid portion of freshly excreted pats (Holter amp Scholtz 2007) Theoffspring of these early dung pat colonizers add complexity to the community Oncesufficient numbers of these coprophages and their larvae have aggregated in the dung pat awave of predatory arthropods respond to this prey source (Koskela amp Hanski 1977) As themoisture evaporates from the dung it becomes less attractive to many of the coprophages(Stevenson amp Dindal 1987) Additionally many coprophages migrate to more recentlydeposited pats (McDaniel Boddicker amp Balsbaugh 1971 Mohr 1943) Predators followthese prey species (Slade et al 2016 Sowig Himmelsbach amp Himmelsbach 1997) This


Figure 4 Correlation of the diversity of dung beetles to total arthropod abundance in cattle dung patsDung beetle diversity (Shannon H) in dung pats was run in a linear regression to observe correlation tototal arthropod abundance per individual cattle dung pat Beginning in June (A) and late July (B) therewas a significant and positive correlation between dung beetle diversity and the total arthropod abundancein dung pats that all species could freely colonize (n= 36 in both A and B)



succession of colonization is supported by observations of arthropods during this studyArthropod abundance decreased as the pats lost moisture and by the time dung was 14 dold the arthropod community metrics and moisture content reached a constant low forthe rest of the observation period These observations resemble the succession of dungcolonization seen in similar studies (Kessler amp Balsbaugh 1972Mohr 1943 Valiela 1969)

In addition to their changes over the age of the pat dung arthropod communities alsochange over the season Due to the resource intensity of this study it was conducted on asingle ranch in a single year which challenges generalizations on seasonal patterns in dungdegradations Nevertheless some trends between the two observation dates are noteworthyIn the early season peak arthropod abundance was in 7 d old dung pats Later in the seasonpeak abundance was in 2 to 4 d old pats with a more gradual decrease in abundance as thepat aged (Fig 2) Several explanations may factor into these patterns of dung colonizationTemperature has an important effect on dung colonization (Errouissi et al 2004) withcolder temperatures affecting colonization and degradation rates In this study early seasonhad a colder temperature (167 C daily average) than late season (211 C daily average)and this may partially explain our experimental results Additionally many arthropodssuch as dung beetles do not share the same phenology with many adults emerging andbecoming active in different times over the grazing season (Pecenka and Lundgren 2018in review) Higher temperatures later in the season would also dry the pat more quicklyand water content of the pat influences its attraction to dung arthropods (Finn amp Giller2000) This higher temperature causes the dung pat to dry at a quicker rate making itless attractive and suitable for dung beetles and other large coprophagous arthropodsAs the grazing season progresses cool season grasses are replaced with warm seasonspecies (Ellis-Felege Dixon amp Wilson 2013) The changes in palatability and digestibility ofdifferent plants to cattle can affect the composition of the dung and its attractiveness toarthropods (Holter 2016) Without further research we cannot definitively say what drovethese slightly different patterns of colonization over the season but these considerationsbecome important to ranchers wanting consistent dung degradation on their land

These results provide further evidence that dung beetles contribute multiple ecosystemfunctions to rangelands by the dung arthropod community (Beynon et al 2012 Manninget al 2016 Nichols et al 2008) Arthropod communities are major contributors to dungdegradation and dung beetle abundance and diversity influence many of the characteristicsof this community (abundance richness and diversity) (Table 2 Fig 4) Dung beetles werestrongly correlated with the overall arthropod community even though they representedonly 15ndash3 of the specimens collected in the study Dung beetles colonize fresh dungpats and feed on the liquid portion of the dung they leave when water becomes limited(Holter amp Scholtz 2007) Dung beetles may also deposit eggs in or underneath the dungpat where their larvae will develop and consume the dried fibrous portion of the dung patthat remains (Laurence 1954) Dung beetles can also alter the dung pat and the arthropodsthat will colonize it Through their tunneling and bioturbation of the dung pat they allowair to reach the center of the pat and cause it to degrade faster by converting it into formsaccessible to plant roots and microbes (Bang et al 2005 Bornemissza 1970 Stevenson ampDindal 1987) We hypothesize that dung beetlesrsquo robust bodies also provide a lsquolsquohighway


systemrsquorsquo that other arthropods such as predatory beetles or spiders can use to search forprey such as pest maggots These tunnels would then also open up the patrsquos interior tothe micro-coprophage community that lack the ability to burrow through the pat furtherincreasing their effect on pat degradation Their impact can be seen in the large amount ofOM lost in the first days of arthropod colonization

CONCLUSIONSbull Degradation of dung pats was increased by 30 (approximately 30 d) when the entireinsect community was present in the patsbull Early colonization was essential to dung degradation Most dung degradation occurredwithin a week of dung deposition and the main effects of insects on pat degradationoccurred within 2 d of pat depositionbull Although dung beetles were only 15ndash30 of the arthropod community in dung theirabundance was strongly correlated with the rest of the community This data supportstheir role as essential contributors to dung degradation

ACKNOWLEDGEMENTSThe authors thank Mike Bredeson Claire LaCanne Amy Lieferman Alexander NikolasCassandra Pecenka and Kassidy Weathers for their assistance in construction deployingand field removal of dung pat cages Special thanks as well to Mark Longfellow in assistingwith insect identification and K Creek Ranch for use of their pasture

ADDITIONAL INFORMATION AND DECLARATIONS

FundingEcdysis Foundation and NCR-SARE via student research grant GNC15-207 funded thisresearch The funders had no role in study design data collection and analysis decision topublish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsEcdysis FoundationNCR-SARE GNC15-207

Competing InterestsJonathan Lundgren is the director of Ecdysis Foundation and CEO of Blue Dasher Farm

Author Contributionsbull Jacob R Pecenka conceived and designed the experiments performed the experimentsanalyzed the data prepared figures andor tables authored or reviewed drafts of thepaper approved the final draftbull Jonathan G Lundgren conceived and designed the experiments analyzed the datacontributed reagentsmaterialsanalysis tools prepared figures andor tables authoredor reviewed drafts of the paper approved the final draft


Data AvailabilityThe following information was supplied regarding data availability

The raw data are provided in Data S1

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj5220supplemental-information

REFERENCESAarons SR OrsquoConnor CR Hosseini HM Gourley CJP 2009 Dung pads increase

pasture production soil nutrients and microbial biomass carbon in grazed dairy sys-tems Nutrient Cycling in Agroecosystems 8481ndash92 DOI 101007s10705-008-9228-5

Anderson JR Merritt RW Loomis EC 1984 The insect-free cattle dropping and itsrelationship to increased dung fouling of rangeland pastures Journal of EconomicEntomology 77133ndash141 DOI 101093jee771133

Bang H Lee J Kwon O Na Y Jang Y KimW 2005 Effects of paracoprid dung beetles(Coleoptera Scarabaeidae) on the growth of pasture herbage and on the underlyingsoil Applied Soil Ecology 29165ndash171 DOI 101016japsoil200411001

Beynon SA Mann DJ Slade EM Lewis OT 2012 Species-rich dung beetle communitiesbuffer ecosystem services in perturbed agro-ecosystems Journal of Applied Ecology491365ndash1372 DOI 101111j1365-2664201202210x

Beynon SAWainwrightWA Christie M 2015 The application of an ecosystemservices framework to estimate the economic value of dung beetles to the U K cattleindustry Ecological Entomology 40(Suppl 1)124ndash135 DOI 101111een12240

Blume RR 1985 A check-list distributional record and annotated bibliography of theinsects associated with bovine droppings on pasture in America north of MexicoSouthwest Entomol 91ndash55

Bornemissza GF 1970 An effect of dung beetle activity on plant yeild Pedobiologia101ndash7

Cervenka VJ Moon RD 1991 Arthropods associated with fresh cattle dung pats inMinnesota Journal of the Kansas Entomological Society 64131ndash145

Cook DF Dadour IR Ali DN 1996 Effect of diet on the excretion profile ofivermectin in cattle faeces International Journal for Parasitology 26291ndash295DOI 1010160020-7519(95)00132-8

Doube BM 1990 A functional classification for analysis of the structure of dung beetleassemblages Ecological Entomology 15371ndash383DOI 101111j1365-23111990tb00820x

Ellis-Felege SN Dixon CSWilson SD 2013 Impacts and management of invasivecool-season grasses in the Northern Great Plains challenges and opportunities forwildlifeWildlife Society Bulletin 37510ndash516

Errouissi FF Haloti S Jay-Robert P Janati-Idrissi A Lumaret JP 2004 Effects of theattractiveness for dung beetles of dung pat origin and size along a climatic gradientEnvironmental Entomology 3345ndash53 DOI 1016030046-225X-33145


Fincher GT 1981 The potential value of dung beetles in pasture ecosystems Journal ofGeorgia Entomological Society 16(Suppl 1)316ndash333

Finn JA Giller PS 2000 Patch size and colonisation patterns an experimental anal-ysis using north temperate coprophagous dung beetles Ecography 23315ndash327DOI 101111j1600-05872000tb00287x

Gillard P 1967 Coprophagous beetles in pasture ecosystems Journal of the AustralianInstitute of Agricultural Science 3330ndash34

Haynes RJ Williams PH 1993 Nutrient cycling and soil fertility in the grazed pastureecosystem Advances in Agronomy 49119ndash199 DOI 101016S0065-2113(08)60794-4

Holter P 1979 Effect of dung-beetles (Aphodius spp) and earthworms on the disap-pearance of cattle dung Oikos 32393ndash402 DOI 1023073544751

Holter P 2016Herbivore dung as food for dung beetles elementary coprology forentomologists Ecological Entomology 41367ndash377 DOI 101111een12316

Holter P Scholtz CH 2007What do dung beetles eat Ecological Entomology32690ndash697 DOI 101111j1365-2311200700915x

Johnston CA 2014 Agricultural expansion land use shell game in the US NorthernPlains Landscape Ecology 2981ndash95 DOI 101007s10980-013-9947-0

Kessler H Balsbaugh EU 1972 Succession of adult Coleoptera in Bovine Manure in EastCentral South Dakota Annals of the Entomological Society of America 651333ndash1336DOI 101093aesa6561333

Koskela H Hanski I 1977 Structure and succession in a beetle community inhabitingcow dung Annales Zoologici Fennici 14204ndash223

Laurence BR 1954 The larval inhabitants of cow pats Journal of Animal Ecology23234ndash260 DOI 1023071982

Lee CMWall R 2006 Cow-dung colonization and decomposition following insectexclusion Bulletin of Entomological Research 96315ndash322 DOI 101079BER2006428

Losey JE VaughanM 2006 Economic value of ecological services provided by insectsBioscience 56311ndash323 DOI 1016410006-3568(2006)56[311TEVOES]20CO2

MacLusky DS 1960 Some estimates of the areas of pasture fouled by the excreta of dairycows Journal of the British Grassland Society 15181ndash188DOI 101111j1365-24941960tb00176x

Macqueen A Beirne P 1975 Effects of cattle dung and dung beetle activity on growthof beardless wheatgrass in British Columbia Canadian Journal of Plant Science55961ndash967 DOI 104141cjps75-152

Manning P Slade EM Beynon SA Lewis OT 2016 Functionally rich dung beetleassemblages are required to provide multiple ecosystem services AgricultureEcosystems amp Environment 21887ndash94 DOI 101016jagee201511007

McDaniel B Boddicker ML Balsbaugh EU 1971 Coleoptera inhabiting bovine manurein a pasture on the Big Sioux river flood plain in South Dakota Proceedings of theSouth Dakota Academy of Sciences 50220ndash237

Merritt RW Anderson JR 1977 The effects of different pasture and rangeland ecosys-tems on the annual dynamics of insects in cattle droppings Hilgardia 4531ndash71DOI 103733hilgv45n02p031


Mohr CO 1943 Cattle droppings as ecological units Ecological Monographs 13275ndash298DOI 1023071943223

National Agricultural Statisitics Service (NASS) 2016 United States Department ofAgriculture Available at httpwwwnassusdagov (accessed on 20 December 2016)

Nichols EE Spector SS Louzada JJ Larsen TT Amezquita SS Favila ME 2008Ecological functions and ecosystem services provided by Scarabaeinae dung beetlesBiological Conservation 1411461ndash1474 DOI 101016jbiocon200804011

Penttila A Slade EM Simojoki A Riutta T Minkkinen K Roslin T 2013 Quantify-ing beetle-mediated effects on gas fluxes from dung pats PLOS ONE 8e71454DOI 101371journalpone0071454

Petersen RG Lucas HLWoodhouseWW 1956 The distribution of excreta by freelygrazing cattle and its influence on pasture fertility I Excretal density AgronomyJournal 48440ndash444 DOI 102134agronj195600021962004800100002x

Ratcliffe BC PaulsenMJ 2008 The Scarabaeoid beetles of Nebraska (ColeopteraScarabaeoidea) Bulletin of the University of Nebraska State Museum 221ndash570

Sanders DP Dobson RC 1966 The insect complex associated with Bovine Ma-nure in Indiana Annals of the Entomological Society of America 59955ndash959DOI 101093aesa595955

Slade EM Roslin T Santalahti M Bell T 2016 Disentangling the lsquobrown worldrsquo faecal-detritus interaction web dung beetle effects on soil microbial properties Oikos125629ndash635 DOI 101111oik02640

Sowig P Himmelsbach R HimmelsbachW 1997 Predatormdashprey relationship betweeninsect larvae growth of Sphaeridium larvae (Coleoptera Hydrophilidae) under timeconstraints through predation on Musca autumnalis maggots (Diptera Muscidae)Canadian Journal of Zoology 752069ndash2076 DOI 101139z97-841

Stevenson BG Dindal DL 1987 Insect effects on decomposition of cow dung inmicrocosms Pedobiologia 3081ndash92

Strong L 1992 Avermectins a review of their impact on insects of cattle dung Bulletin ofEntomological Research 82265ndash274 DOI 101017S0007485300051816

Suarez VH Lifschitz AL Sallovitz JM Lanusse CE 2003 Effects of ivermectin anddoramectin faecal residues on the invertebrate colonization of cattle dung Journalof Applied Entomology 127481ndash488 DOI 101046j0931-2048200300780x

Tixier T Lumaret JP Sullivan GT 2015 Contribution of the timing of the successivewaves of insect colonisation to dung removal in a grazed agro-ecosystem EuropeanJournal of Soil Biology 6988ndash93 DOI 101016jejsobi201506001

[USDA-NRCS] United States Department of Agriculture-Natural Resources Con-servation Service 2016Web soil survey Web-based document Available at httpwwwwebsoilsurveynrcsusdagov (accessed on 28 December 2016)

Triplehorn CA Johnson NF 2005 Borror and DeLongrsquos introduction to the study ofinsects Seventh Edition Pacific Grove Thomson BrooksCole

Valiela I 1969 The arthropod fauna of bovine dung in central New York and sources onits natural history Journal of the New York Entomological Society 77210ndash220


WeedaWC 1967 The effect of cattle dung patches on pasture growth botanicalcomposition and pasture utilisation New Zealand Journal of Agricultural Research10150ndash159 DOI 10108000288233196710423087

Wright CKWimberly MC 2012 Recent land use change in the Western Corn Beltthreatens grasslands and wetlands Proceedings of the National Academy of Sciencesof the United States of America 1104134ndash4139

WuX Sun S 2010 The roles of beetles and flies in yak dung removal in an alpinemeadow of eastern Qinghai-Tibetan Plateau Ecoscience 17146ndash155DOI 10298017-2-3319

Yamada D Imura O Shi K Shibuya T 2007 Effect of tunneler dung beetles oncattle dung decomposition soil nutrients and herbage growth Grassland Science53121ndash129 DOI 101111j1744-697X200700082x


(Weeda 1967) Dung loses 22 (but up to 80) of its nitrogen (N) to volatilization within60 d of deposition (Nichols et al 2008 Weeda 1967) Other important nutrients such asphosphorus (P) and potassium (K) are present in dung pats in much smaller quantities andcan be lost to leaching and runoff when left on the soil surface (Gillard 1967 Nichols et al2008 Petersen Lucas amp Woodhouse 1956) Volatilization and reductions of these elementsdecreases the nutrient availability to the plant community resulting in lower quantity andquality of forage for future cattle grazing (Aarons et al 2009 Bang et al 2005)

A variety of factors affect how quickly dung is incorporated into the soil Reports ofdung degradation rates vary from 50ndash65 d over the season (Holter 1979) 57ndash78 d in latespring to 88ndash111 d in late summer (Lee amp Wall 2006) and up to 3 y in cattle grazingsystems with high insecticide use (Anderson Merritt amp Loomis 1984 Strong 1992) Thisvariability is due to factors that include weather (Holter 1979) seasonality (Lee amp Wall2006) insecticide use (Suarez et al 2003) and the nutritional quality of the dung itself(Cook Dadour amp Ali 1996) Degradation of dung pats is facilitated by arthropods thataccelerate the incorporation of the dung pat organic matter into the soil and improvesoilrsquos aeration and water holding capacity (Macqueen amp Beirne 1975) Dung often supportsdozens or even hundreds of arthropod species (Blume 1985 Merritt amp Anderson 1977Valiela 1969)

Arthropods that colonize dung pats can be categorized into different functional guildsthat each contribute to the eventual incorporation of the dung into the soil One ofthe first studies that considered dung community function was Mohr (1943) whichprompted other studies that documented arthropod succession in a dung pat and theirvarying niches within the micro-habitat (Cervenka amp Moon 1991 Koskela amp Hanski 1977Sanders amp Dobson 1966) These studies are accompanied by more recent explorationsof the importance of dung beetles (Scarabaeidae) and the multiple ecosystem servicesthat they provide (Beynon et al 2012 Manning et al 2016 Nichols et al 2008) One ofthese ecosystem services is dung beetlesrsquo ability to increase the productivity of rangelandecosystems (Bang et al 2005 Penttila et al 2013) Increased rangeland productivity isachieved by bioturbation and burial of dung that results in capturing ephemeral nutrientsfor surrounding forage plants up to 127 cm away from the dung pat (Bornemissza 1970Macqueen amp Beirne 1975 Yamada et al 2007) A second important ecosystem service isthe suppression of dung inhabiting pests to grazing cattle (Fincher 1981) By removingnutritional resources and habitat dung beetles reduce pest maggot abundance (Doube1990 Nichols et al 2008) Suppressing these pests is accelerated when natural enemiessuch as predatory staphylinid or hister beetles and parasitoid wasps colonize the dungpat (Cervenka amp Moon 1991) These ecosystem services provided by dung beetles (as wellas other members of the dung arthropod community) have an economic value to theranching operation (Beynon Wainwright amp Christie 2015) but most of the numbers usedto generate these values are at least 37 years old (Beynon et al 2012 Fincher 1981 Losey ampVaughan 2006)

The goal of our study was to document the dung insect community in eastern SouthDakota and determine dung degradation rates over time in the presence and absenceof this community Cages like those employed here help to isolate the contribution of


































































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The importance of dung beetles and arthropod communities ... · dung pat and arthropod characteristics including pat wet weight, dry weight, moisture content, organic matter content,

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