Dung beetle–mammal associations: methods, research trends and future directions

Dung beetles are increasingly used as a study taxon—both as bioindicators of environmental change, and as a model system for exploring ecosystem functioning. The advantages of this focal taxon approach are many; dung beetles are abundant in a wide range of terrestrial ecosystems, speciose, straightforward to sample, respond to environmental gradients and can be easily manipulated to explore species-functioning relationships. However, there remain large gaps in our understanding of the relationship between dung beetles and the mammals they rely on for dung. Here we review the literature, showing that despite an increase in the study of dung beetles linked to ecosystem functioning and to habitat and land use change, there has been little research into their associations with mammals. We summarize the methods and findings from dung beetle–mammal association studies to date, revealing that although empirical field studies of dung beetles rarely include mammal data, those that do, indicate mammal species presence and composition has a large impact on dung beetle species richness and abundance. We then review the methods used to carry out diet preference and ecosystem functioning studies, finding that despite the assumption that dung beetles are generalist feeders, there are few quantitative studies that directly address this. Together this suggests that conclusions about the effects of habitat change on dung beetles are based on incomplete knowledge. We provide recommendations for future work to identify the importance of considering mammal data for dung beetle distributions, composition and their contributions to ecosystem functioning; a critical step if dung beetles are to be used as a reliable bioindicator taxon.

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Dung beetle community assemblages in a southern African landscape: niche overlap between domestic and wild herbivore dung

Bulletin of Entomological Research ◽

10.1017/s0007485321000742 ◽

2021 ◽

pp. 1-12

Author(s):

B. Sands ◽

N. Mgidiswa ◽

S. Curson ◽

C. Nyamukondiwa ◽

R. Wall

Keyword(s):

Niche Overlap ◽

Dung Beetle ◽

Dung Beetles ◽

Sub Saharan Africa ◽

Cattle Dung ◽

Mammal Species ◽

Wide Range ◽

Domestic Livestock ◽

Abundance And Diversity ◽

Diurnal Species

Abstract Dung beetles provide important ecosystem functions in semiarid environments, improving the physiochemical characteristics of the soil through tunnelling and burying nutrient-rich dung. In sub-Saharan Africa, diverse indigenous mammal communities support highly abundant dung beetle populations in savannah ecosystems. However, the conversion of landscapes to livestock agriculture may result in changes in the abundance and diversity of wild mammal species. This is likely to have significant impacts on dung beetle communities, particularly because domestic livestock dung may be contaminated with toxic residues of veterinary parasiticides. The environmental impact is likely to be affected by the degree of niche overlap between the beetle communities that colonize cattle dung and those that colonize the dung of wild mammals. We compared dung beetle communities between a pristine national park habitat dominated by large wild herbivores, and a pastoral farming community dominated by domestic livestock. Diurnal dung beetles were attracted to cattle dung in greater abundance and diversity compared to elephant, zebra or giraffe dung. Nocturnal/crepuscular dung beetles were attracted to non-ruminant dung (elephant and zebra) in higher abundance compared to ruminant dung (cattle and giraffe). Although there were no clear trophic specializations, three diurnal species showed an association with cattle dung, whereas eight nocturnal/crepuscular species showed an association with non-ruminant (elephant and zebra) dung. Diurnal species may be at greater risk from the toxic effects of residues of veterinary parasiticides in domestic livestock dung. Although many species showed trophic associations with wild herbivore dung, these beetles can utilize a wide range of dung and will readily colonize cattle dung in the absence of other options. As more land is converted to livestock agriculture, the contamination of dung with toxic residues from veterinary parasiticides could therefore negatively impact the majority of dung beetle species.

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Dung beetles as vertebrate samplers – a test of high throughput analysis of dung beetle iDNA

10.1101/2021.02.10.430568 ◽

2021 ◽

Author(s):

Rosie Drinkwater ◽

Elizabeth L. Clare ◽

Arthur Y. C. Chung ◽

Stephen J. Rossiter ◽

Eleanor M. Slade

Keyword(s):

High Throughput ◽

High Throughput Sequencing ◽

Dung Beetle ◽

Blood Feeding ◽

Preliminary Evidence ◽

Dung Beetles ◽

High Throughput Analysis ◽

Humid Forest ◽

Terrestrial Vertebrates ◽

Wide Range

AbstractThe application of environmental DNA (eDNA) sampling in biodiversity surveys has gained widespread acceptance, especially in aquatic systems where free eDNA can be readily collected by filtering water. In terrestrial systems, eDNA-based approaches for assaying vertebrate biodiversity have tended to rely on blood-feeding invertebrates, including leeches and mosquitoes (termed invertebrate-derived DNA or iDNA). However, a key limitation of using blood-feeding taxa as samplers is that they are difficult to trap, and, in the case of leeches, are highly restricted to humid forest ecosystems. Dung beetles (superfamily Scarabaeoidea) feed on the faecal matter of terrestrial vertebrates and offer several potential benefits over blood-feeding invertebrates as samplers of vertebrate DNA. Importantly, these beetles can be easily captured in large numbers using simple, inexpensive baited traps; are globally distributed; and also occur in a wide range of biomes, allowing mammal diversity to be compared across habitats. In this exploratory study, we test the potential utility of dung beetles as vertebrate samplers by sequencing the mammal DNA contained within their guts. First, using a controlled feeding experiment, we show that mammalian DNA can be retrieved from the guts of large dung beetles (Catharsius renaudpauliani) for up to 10 hours after feeding. Second, by combining high-throughput sequencing of a multi-species assemblage of dung beetles with PCR replicates, we show that multiple mammal taxa can be identified with high confidence. By providing preliminary evidence that dung beetles can be used as a source of mammal DNA, our study highlights the potential for this widespread group to be used in future biodiversity monitoring surveys.

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Dung beetles as samplers of mammals in Malaysian Borneo—a test of high throughput metabarcoding of iDNA

PeerJ ◽

10.7717/peerj.11897 ◽

2021 ◽

Vol 9 ◽

pp. e11897

Author(s):

Rosie Drinkwater ◽

Joseph Williamson ◽

Elizabeth L. Clare ◽

Arthur Y.C. Chung ◽

Stephen J. Rossiter ◽

...

Keyword(s):

Mammalian Species ◽

Dung Beetle ◽

Blood Feeding ◽

Iucn Red List ◽

Dung Beetles ◽

Gut Contents ◽

Terrestrial Vertebrates ◽

Wide Range ◽

Potential Benefits ◽

Short Time

Invertebrate-derived DNA (iDNA) sampling in biodiversity surveys is becoming increasingly widespread, with most terrestrial studies relying on DNA derived from the gut contents of blood-feeding invertebrates, such as leeches and mosquitoes. Dung beetles (superfamily Scarabaeoidea) primarily feed on the faecal matter of terrestrial vertebrates and offer several potential benefits over blood-feeding invertebrates as samplers of vertebrate DNA. Importantly, these beetles can be easily captured in large numbers using simple, inexpensive baited traps, are globally distributed, and occur in a wide range of habitats. To build on the few existing studies demonstrating the potential of dung beetles as sources of mammalian DNA, we subjected the large-bodied, Bornean dung beetle (Catharsius renaudpauliani) to a controlled feeding experiment. We analysed DNA from gut contents at different times after feeding using qPCR techniques. Here, we first describe the window of DNA persistence within a dung beetle digestive tract. We found that the ability to successfully amplify cattle DNA decayed over relatively short time periods, with DNA copy number decreasing by two orders of magnitude in just 6 h. In addition, we sampled communities of dung beetles from a lowland tropical rainforest in Sabah, Malaysia, in order to test whether it is possible to identify vertebrate sequences from dung beetle iDNA. We sequenced both the gut contents from large dung beetle species, as well as whole communities of smaller beetles. We successfully identified six mammalian species from our samples, including the bearded pig (Sus barbatus) and the sambar deer (Rusa unicolor)—both vulnerable species on the IUCN red list. Our results represent the first use of dung beetle iDNA to sample Southeast Asian vertebrate fauna, and highlight the potential for dung beetle iDNA to be used in future biodiversity monitoring surveys.

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Seasonality, dung specificity and competition in dung beetle assemblages in the Australian Wet Tropics, north-eastern Australia

Journal of Tropical Ecology ◽

10.1017/s026646740400224x ◽

2005 ◽

Vol 21 (1) ◽

pp. 1-8 ◽

Cited By ~ 19

Author(s):

Karl Vernes ◽

Lisa C. Pope ◽

Christopher J. Hill ◽

Felix Bärlocher

Keyword(s):

Null Model ◽

Dung Beetle ◽

Dung Beetles ◽

Maximum Temperature ◽

Wet Season ◽

Habitat Types ◽

Mammal Species ◽

Eastern Australia ◽

Species Effect ◽

Wet Tropics

A trapping study of five mammal species in wet sclerophyll forest adjacent to rain forest in the Australian Wet Tropics was used to examine the seasonal diversity, abundance and dung-specificity of dung beetles associated with mammal dung. A total of 542 dung beetles from 11 species within three genera was recovered from beneath the traps of 1104 mammal captures. The diversity of beetles associated with the dung of the northern bettong (Bettongia tropica), a mycophagous marsupial, differed significantly from the diversity predicted by a null model. Numbers of beetles varied significantly with type of dung, indicating preference by beetles. Beetle numbers were related positively to a 1-mo lag in monthly mean minimum temperature and less strongly to maximum temperature and rainfall. Significantly more beetles per mammal capture were detected in the wet season than in the dry season. Dung beetles showed a strong preference for either the Eucalyptus woodland (six species) or the adjacent Allocasuarina forest (four species), with only one species occurring in both habitat types. Beetle species from the Eucalyptus woodland were typically only detected in the late wet and early dry seasons, while species in the wetter Allocasuarina forest were generally collected during the late dry and early wet seasons. A significant ‘checkerboard’ species effect was detected in both time and space in both habitat types, suggesting that competition for dung was strong.

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Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0150 ◽

2016 ◽

Vol 283 (1831) ◽

pp. 20160150 ◽

Cited By ~ 32

Author(s):

Tobin J. Hammer ◽

Noah Fierer ◽

Bess Hardwick ◽

Asko Simojoki ◽

Eleanor Slade ◽

...

Keyword(s):

Greenhouse Gas Emissions ◽

Greenhouse Gas ◽

Antibiotic Treatment ◽

Methanogenic Archaea ◽

Dung Beetle ◽

Dung Beetles ◽

Gas Emissions ◽

Antibiotic Effect ◽

Wide Range ◽

Survival And Reproduction

Antibiotics are routinely used to improve livestock health and growth. However, this practice may have unintended environmental impacts mediated by interactions among the wide range of micro- and macroorganisms found in agroecosystems. For example, antibiotics may alter microbial emissions of greenhouse gases by affecting livestock gut microbiota. Furthermore, antibiotics may affect the microbiota of non-target animals that rely on dung, such as dung beetles, and the ecosystem services they provide. To examine these interactions, we treated cattle with a commonly used broad-spectrum antibiotic and assessed downstream effects on microbiota in dung and dung beetles, greenhouse gas fluxes from dung, and beetle size, survival and reproduction. We found that antibiotic treatment restructured microbiota in dung beetles, which harboured a microbial community distinct from those in the dung they were consuming. The antibiotic effect on beetle microbiota was not associated with smaller size or lower numbers. Unexpectedly, antibiotic treatment raised methane fluxes from dung, possibly by altering the interactions between methanogenic archaea and bacteria in rumen and dung environments. Our findings that antibiotics restructure dung beetle microbiota and modify greenhouse gas emissions from dung indicate that antibiotic treatment may have unintended, cascading ecological effects that extend beyond the target animal.

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Species composition and community structure of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) compared among savanna and forest formations in the southwestern Brazilian Cerrado

Zoologia (Curitiba) ◽

10.3897/zoologia.37.e58960 ◽

2020 ◽

Vol 37 ◽

pp. 1-12

Author(s):

Jorge Luiz da Silva ◽

Ricardo José da Silva ◽

Izaias Médice Fernandes ◽

Wesley Oliveira de Sousa ◽

Fernando Zagury Vaz-de-Mello

Keyword(s):

Species Richness ◽

Species Diversity ◽

Deciduous Forest ◽

Dung Beetle ◽

Dung Beetles ◽

Gallery Forest ◽

Brazilian Cerrado ◽

Habitat Types ◽

Mato Grosso ◽

Species Richness And Abundance

Although dung beetles are important members of ecological communities and indicators of ecosystem quality, species diversity, and how it varies over space and habitat types, remains poorly understood in the Brazilian Cerrado. We compared dung beetle communities among plant formations in the Serra Azul State Park (SASP) in the state of Mato Grosso, Brazil. Sampling (by baited pitfall and flight-interception traps) was carried out in 2012 in the Park in four habitat types: two different savanna formations (typical and open) and two forest formations (seasonally deciduous and gallery). A total of 5,400 individuals collected comprised 57 species in 22 genera. Typical savanna had the greatest species richness and abundance, followed by open savanna and deciduous forest, while the gallery forest had the fewest species but high abundance. Tunnelers (one of three main nesting behavior guilds) showed the greatest richness and abundance (except in the gallery forest, where one dweller species was extremely abundant) in all plant formations. We found that species richness and abundance of the dung beetle community are influenced by differences among plant formations. Habitat heterogeneity in the different plant formations along with anthropic influences (fire, habitat fragmentation) are cited as important factors that explain guild and species richness and distribution patterns. These results emphasize the importance of protected areas, such as SASP, for the maintenance and conservation of species diversity in the Brazilian Cerrado.

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Spatiotemporal effects on dung beetle activities in island forests-home garden matrix in a tropical village landscape

Scientific Reports ◽

10.1038/s41598-021-96831-5 ◽

2021 ◽

Vol 11 (1) ◽

Cited By ~ 1

Author(s):

G. Asha ◽

K. Manoj ◽

P. P. Megha ◽

Palatty Allesh Sinu

Keyword(s):

Species Composition ◽

Functional Groups ◽

Dung Beetle ◽

Dung Beetles ◽

Home Gardens ◽

Home Garden ◽

Sacred Groves ◽

Open Habitat ◽

Wide Range ◽

Closed Habitat

AbstractInsects in seasonal tropics experience a wide range of temperatures along seasons, habitats, and a day. Therefore, the thermal tolerance of the insects can be a major driver for their habitat preference, temporal patterns of activity, and formation of communities. We examined the dung beetle communities of eleven pairs of neighboring open (home gardens) and closed habitats (sacred groves) during dry and wet seasons and diel periods (day and night) to understand the dung beetle activities along a spatiotemporal gradient constituted by the sacred groves—home garden matrix on a tropical village landscape. We tested the following hypotheses: (i) closed habitats have greater activities of dung beetles over open habitats; (ii) the diurnal communities of dung beetles are different from the nocturnal communities; and (iii) the diurnal-nocturnal activities of dung beetles could be predicted by the habitat and season. We considered abundance, richness, total biomass, and Shannon diversity of overall beetles, abundance of different functional groups, and species composition in communities as the quantitative measures in the predictive statistical models. In total, 2727 dung beetles belonging to 38 species, ten genera, and three functional groups were collected. The open habitat supported more number of dung beetles (N = 2318) than the closed habitat (N = 409). The diurnal communities were different from nocturnal communities, particularly in open habitat, where the temperature was different between day and night. The dominant species of the diurnal communities of open habitat hardly used the closed habitat in any context including dry–wet seasons, but the nocturnal communities of the open habitat were closer to the communities of closed habitat. The diel period and habitat predicted the abundance activity of functional groups; season was a poor predictor of dung beetle activities. Given that the species composition has turned over across habitats, and the closed habitat supported remarkably lesser number of beetles than the open habitats, the closed habitat is unlikely to be a thermal refuge for the open habitat species in village landscapes that have island forests, such as sacred groves, and home gardens form a matrix.

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Metagenomic sequencing of dung beetle intestinal contents directly detects and identifies mammalian fauna

10.1101/074849 ◽

2016 ◽

Cited By ~ 3

Author(s):

Conrad P.D.T. Gillett ◽

Andrew J. Johnson ◽

Iain Barr ◽

Jiri Hulcr

Keyword(s):

High Throughput Sequencing ◽

Sequence Data ◽

Sampling Site ◽

Dung Beetle ◽

Dung Beetles ◽

List Type ◽

Metagenomic Sequencing ◽

Biodiversity Assessment ◽

Mammal Species ◽

Intestinal Contents

SummaryCost, time, and expertise constraints limit traditional observation-based comprehensive biodiversity assessment. Therefore, surrogate focal taxa representative of wider biodiversity are commonly used as an imperfect ‘proxy’. Contemporary biodiversity assessments are also increasingly benefiting from the combination of high-throughput sequencing and metagenomic methodologies that enable identification of environmental DNA samples. However, there is a need for empirical studies combining the use of surrogate taxa with metagenomic approaches, that promise rapid and efficient biodiversity assessment.We here tested for the first time the possibility of using the intestinal contents of wild-collected dung beetles (Scarabaeidae) as a source of mammalian DNA, in a metagenomics proof-of-concept approach to directly detect and identify mammals from an area of savanna-scrub in southern Africa. Dung beetles have been purveyed as an indirect proxy measure of mammalian diversity, owing to their dependence upon vertebrate dung as a food source, and the ease with which they can be comprehensively sampled using simple and repeatable trapping protocols, achievable much faster than vertebrate surveys.Following shotgun sequencing of gut content DNA extractions from ten dung beetle species, we usedin silicofilters to identify mammals by searching the resulting reads against known mammalian mitochondrial DNA from online sequence repositories, matching 546 paired reads to known mitogenomes held in GenBank, and 634 reads to known mammal barcode sequences held in BOLD. Identified mammalian sequences were consistent with wild and domesticated ungulates known from the sampling site, and included blue wildebeest, plains zebra, and domestic cattle and goat. Four dung beetle samples yielded sufficient sequence data to successfully assemble the near-complete mitogenome of blue wildebeest at up to 21 X mean coverage, despite low initial DNA concentrations, unambiguously corroborating identification.It is conceptually and practically possible to rapidly and economically apply metagenomic techniques in dung beetle gut sequencing to detect the presence of mammals upon whose dung the beetles have fed. Since the approach can be readily scaled up, it may prove to be of practical use as a complement to traditional biodiversity assessment methods, and should be tested in usefulness for detecting rare, endangered or cryptic mammal species.

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Strong Association between Serotonin Transporter 5-HTTVNTR Variant and Psychoactive Substance (Nicotine) Use in the Turkish Cypriot Population

Current Drug Metabolism ◽

10.2174/1389200221666200620201348 ◽

2020 ◽

Vol 21 (6) ◽

pp. 466-470

Author(s):

Emine Kandemis ◽

Gulten Tuncel ◽

Ozen Asut ◽

Sehime G. Temel ◽

Mahmut C. Ergoren

Keyword(s):

Serotonin Transporter ◽

Association Studies ◽

Strong Association ◽

Smoking Behavior ◽

Population Based ◽

Genome Wide Association Studies ◽

Genotype Distribution ◽

Psychological Traits ◽

Wide Range ◽

Turkish Cypriot

Background: The use of psychoactive substances is one of the most dangerous social problems worldwide. Nicotine dependence results from the interaction between neurobiological, environmental and genetic factors. Serotonin is a neurotransmitter that has a wide range of central nervous system activities. The serotonin transporter gene has been previously linked to psychological traits. Objective: A variable number of tandem repeats within the serotonin transporter-linked polymorphic gene region are believed to alter the transcriptional efficiency of the 5-HTT gene. Therefore, we aimed to investigate the association between this polymorphic site and smoking behavior in the Turkish Cypriot population. Methods: A total of 259 (100 smokers, 100 non-smokers and 59 ex-smokers) Turkish Cypriots were included in this population-based cross-sectional study. Genomic DNA was extracted from peripheral blood samples and the 5-HTTVNTR2 polymorphisms were determined by the PCR-RFLP. Results: The allelic frequency and genotype distribution results of this study showed a strong association (P<0.0001) between smokers and non-smokers. No statistical significance was found between non-smokers and ex-smokers. Conclusion: This is the first genetic epidemiology study to investigate the allelic frequencies of 5-HTTVNTR2 polymorphisms associated with smoking behavior in the Turkish Cypriot population. Based on the results of this study, genome-wide association studies should be designed for preventive medicine in this population.

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Wood Pastures: A Transitional Habitat between Forests and Pastures for Dung Beetle Assemblages

Forests ◽

10.3390/f12010025 ◽

2020 ◽

Vol 12 (1) ◽

pp. 25

Author(s):

László Somay ◽

Viktor Szigeti ◽

Gergely Boros ◽

Réka Ádám ◽

András Báldi

Keyword(s):

Functional Group ◽

Animal Health ◽

Habitat Type ◽

Dung Beetle ◽

Dung Beetles ◽

Livestock Grazing ◽

Pitfall Traps ◽

Assemblage Composition ◽

Beetle Assemblages

Wood pastures are home to a variety of species, including the dung beetle. Dung beetles are an important functional group in decomposition. Specifically, in terms of livestock manure, they not only contribute to nutrient cycling but are key players in supporting human and animal health. Dung beetles, however, are declining in population, and urgent recommendations are needed to reverse this trend. Recommendations need to be based on solid evidence and specific habitats. Herein, we aimed to investigate the role of an intermediate habitat type between forests and pastures. Wood pastures are key areas for dung beetle conservation. For this reason, we compared dung beetle assemblages among forests, wood pastures, and grasslands. We complemented this with studies on the effects of dung type and season at three Hungarian locations. Pitfall traps baited with cattle, sheep, or horse dung were used in forests, wood pastures, and pasture habitats in spring, summer, and autumn. Dung beetle assemblages of wood pastures showed transient characteristics between forests and pastures regarding their abundance, species richness, Shannon diversity, assemblage composition, and indicator species. We identified a strong effect of season and a weak of dung type. Assemblage composition proved to be the most sensitive measure of differences among habitats. The conservation of dung beetles, and the decomposition services they provide, need continuous livestock grazing to provide fresh dung, as well as the maintenance of wood pastures where dung beetle assemblages typical of forests and pastures can both survive.

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