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Attraction of dung beetles to herbivore dung and synthetic compounds in a comparative field study

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Attraction of dung beetles to herbivore dung and synthetic compounds in a comparative field study

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Dung beetles use a variety of vertebrate dung to provision their offspring. To locate these resources, dung beetles use volatile substances emitted from dung as cues. Although it has been shown in laboratory tests that dung beetles are able to discriminate between different dung types using dung volatiles as kairomones, the attraction of particular dung volatiles and their potential role in resource partitioning of dung types have never been tested in field experiments. For the present study, we conducted field experiments in Austria and two regions in Argentina using pitfall traps baited with either herbivore dung types or synthetic compounds of the dung bouquet (butyric acid, 2-butanone, skatole, indole, and blends of these compounds) to investigate which components or simple mixtures are cues for several taxa of dung beetles. Additionally, we analyzed the degree of specialization of dung beetle species and communities on particular scent types and herbivore dung. Our results show that butyric acid in particular is an important volatile cue for dung beetles. Dung beetles show a preference for some scent types, but turned out to be generalists. This finding is in congruence with the assumption that organisms living from ephemeral resources should rather be generalists instead of specialists.
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... As dung beetles respond rapidly to habitat change (Frank et al., 2017;Gardner et al., 2008;Slade et al., 2011), land use can impair dung removal, for example when species with a high contribution to removal get lost (Dangles et al., 2012;Kaartinen et al., 2013;. Being mobile organisms with highly efficient olfaction (Larsen & Forsyth, 2005;Wurmitzer et al., 2017), for which the location of patchy and unpredictable dung resources is crucial for reproductive success, dung beetles can be easily sampled in a standardized way, which makes them established indicator organisms (Gardner et al., 2008;Hanski & Cambefort, 1991). ...
... Even though habitat selection of dung beetles can occur at small spatial scales (Perrin et al., 2021), the experimental gaps are potentially too small and open patches in forests too sparse to provide habitat for open land species. Being organisms depending on a scarce and patchy resource (Hanski & Cambefort, 1991) equipped with highly efficient olfaction to locate dung (Wurmitzer et al., 2017), these open land species could be promoted by opening forest canopies (Ambrožová et al., 2022;Nichols et al., 2007) and should at least theoretically be able to disperse into gaps. An alternative explanation for the limited functional substitution is that in particular large-bodied open land species have declined in Central Europe during the last decades due to intensified land use (Buse et al., 2018;Buse & Entling, 2020), while communities in forests have maintained their large species that have a high contribution to dung removal (Nervo et al., 2014). ...
... Dung beetle biomass, in turn, increased with temperature due to higher activity of ectothermic organisms in warm weather (Prather et al., 2018). Also, volatile emission from dung is temperature-depended, providing more olfactory cues and easing resource finding at higher temperatures (Wurmitzer et al., 2017). ...
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Ecosystem functioning may directly or indirectly – via change in biodiversity – respond to land use. Dung removal is an important ecosystem function central for the decomposition of mammal faeces, including secondary seed dispersal and improved soil quality. Removal usually increases with dung beetle diversity and biomass. In forests, dung removal can vary with structural variables that are, however, often interrelated, making experiments necessary to understand the role of single variables on ecosystem functions. How gaps and deadwood, two main outcomes of forest management influence dung removal, is unknown. We tested if dung removal responds to gap creation and deadwood provisioning or if treatment effects are mediated via responses of dung beetles. We expected lower removal rates in gaps due to lower dung beetle biomass and diversity. We sampled dung beetles and measured dung removal in a highly‐replicated full‐factorial forest experiment established at 29 sites in three regions of Germany (treatments: Gap, Gap+Deadwood, Deadwood, Control). All gaps were experimentally created and had a diameter of around 30 m. Dung beetle diversity, biomass and dung removal were each lower in gaps than in controls. Dung removal decreased from 61.9% in controls to 48.5% in gaps, irrespective of whether or not the gap had deadwood. This treatment effect was primarily driven by dung beetle biomass but not diversity. Furthermore, dung removal was reduced to 56.9% in the deadwood treatment. Our findings are not consistent with complementarity effects of different dung beetle species linked to biodiversity‐ecosystem functioning relationships that have been shown in several ecosystems. In contrast, identity effects can be pronounced: gaps reduced the abundance of a large‐bodied key forest species (Anoplotrupes stercorosus), without compensatory recruitment of open land species. While gaps and deadwood are important for many forest organisms, dung beetles and dung removal respond negatively. Our results exemplify how experiments can contribute to test hypotheses on the interrelation between land use, biodiversity and ecosystem functioning.
... Most species of dung beetles subsist on excrement from a range of animal species and are thus considered generalists [4]. The ability of dung beetles to sense and navigate to dung pats is dependent on the olfactory response to volatile organic compounds (VOCs) from dung [5][6][7]. These VOCs typically reveal the location, type, and condition of unpredictable and patchily distributed food resources for dung-feeding organisms [8,9]. ...
... Behavioral experiments have confirmed that odors emanating from dung are involved in resource selection by dung beetles; in laboratory assays conducted by Dormont et al. [5,18], dung beetles preferentially oriented toward volatiles from the same dung type they were attracted to in the field. Several reports suggest that traps baited with compounds identified in dung headspace using gas chromatography coupled with mass spectrometry (GC-MS) [7,[18][19][20] were attractive to dung beetles [6,18,19,21]. Recently, a study confirmed the capacity of cattle dung VOCs to alter the composition of dung-inhabiting insect assemblages [22]. ...
... However, studies to more fully characterize livestock dung volatilomes remain limited. Against this research background conducted chiefly in a European setting [6,8,19,25,26], we sought to develop a more complete understanding of dung volatilomes that utilized recent advances in GC-MS to characterize livestock dung from an Australian perspective. Our intention was to provide more robust empirical evidence for use of VOCs by dung beetles when discriminating among dung resources through behavioral assays, volatile analysis, and electroantennography for the first time. ...
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Volatile cues can play a significant role in the location and discrimination of food resources by insects. Dung beetles have been reported to discriminate among dung types produced by different species, thereby exhibiting behavioral preferences. However, the role of volatile organic compounds (VOCs) in dung localization and preference remains largely unexplored in dung beetles. Here we performed several studies: firstly, cage olfactometer bioassays were performed to evaluate the behavioral responses of Bubas bison (Coleoptera: Scarabaeidae) to VOCs emanating from fresh horse, sheep, and cattle dung; secondly, concurrent volatilome analysis was performed to characterize volatilomes of these dung types. Bubas bison adults exhibited greater attraction to horse dung and less attraction to cattle dung, and they preferred dung from horses fed a pasture-based diet over dung from those fed lucerne hay. Volatilomes of the corresponding dung samples from each livestock species contained a diverse group of alkanes, alkenes, alkynes, alcohols, aldehydes, ketones, esters, phenols, and sulfurous compounds, but the composition and abundance of annotated VOCs varied with dung type and livestock diet. The volatilome of horse dung was the most chemically diverse. Results from a third study evaluating electroantennogram response and supplementary olfactometry provided strong evidence that indole, butyric acid, butanone, p-cresol, skatole, and phenol, as well as toluene, are involved in the attraction of B. bison to dung, with a mixture of these components significantly more attractive than individual constituents.
... Dung beetles live in a variety of habitats -pastures, forests, deserts -and have different foraging and soil-nesting behaviour; however, they all rely on dung. Although different dung beetle species may have certain trophic preferences or are attracted to dung from different origins (omnivores, ruminants, monogastric herbivores, etc.), most have a large trophic spectrum (Martín-Piera and Lobo 1996;Dormont et al. 2007;Wurmitzer et al. 2017). Dung attractiveness also partly depends on climatic conditions (Errouissi et al. 2004). ...
... From field experience, 24 h was determined as the smallest amount of time required to get a picture of the dung beetle community; in this amount of time, trapped beetles were not able to escape the trap in order to get eDNA signatures in the NDC device. In each trap, we used 300 g of cow dung as bait to draw the maximum amount of the dung beetle community into the traps, as this resource is highly attractive (Wurmitzer et al. 2017). ...
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The current biodiversity crisis calls for rapid and wide-ranging surveys to assess living organisms. However, some taxa are more elusive than others, making monitoring challenging. This is the case for soil invertebrates, but new molecular technologies such as eDNA metabarcoding could help to alleviate this problem. In this study, we evaluated the feasibility of using an eDNA approach to survey dung beetles, adapting existing monitoring methods for surveying dung fauna to enable eDNA collection in a non-destructive way. The main design idea is to capture species secretions and excretions from a serum-soaked nonwoven compress in a baited non-destructive trap. While the attractiveness of the device to dung beetles and the sampling protocol would benefit from further development, eDNA allowed the identification of more than 68% of trapped species and an identification of relative abundance match rate of 79%. The results of the study demonstrate the effectiveness of eDNA-based detection tools for the monitoring of dung beetles compared to standard surveying and identification techniques. Moreover, the adapted collecting device developed for the study could be used for similar surveys of other terrestrial invertebrates or even re-adapted. Ultimately, we hope this study encourages more non-invasive studies of insects by enabling others to utilize these emerging, non-destructive molecular techniques and therefore foster wide insect monitorings and conservation programs. Implications for insect conservation Standardization and optimization of sampling protocols for inventorying and monitoring is key to unlock invertebrates’ studies and conservation evaluations. Here we show how molecular tools, such as eDNA, are a promising way to gather rapidly ecological information without killing targeted populations by adapting traditional inventory tools. Newly developed NDC traps for dung beetles, inspired by CSR traps, allowed qualitative and quantitative information gathering in temperate agropastoral ecosystems opening the way to large scale eDNA monitoring to inform management and conservation schemes.
... Dung beetles are assumed to be generalists because they depend on ephemeral and patchily distributed resources. However, recent studies suggest that dung beetles are more attracted to the feces of omnivorous mammals than of herbivorous mammals or birds (Wurmitzer et al., 2017). In the present study, even though capuchins are omnivorous and howlers herbivorous, burial probability was significantly higher for seeds embedded in howler feces (40% higher for all bead sizes). ...
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The loss of larger frugivores alters seed dispersal. Species reintroductions have been proposed as a strategy for reversing local disperser extinctions. However, their effects on ecological processes have seldom been assessed. Howler monkeys (Alouatta guariba) have been reintroduced in Tijuca National Park, a defaunated Atlantic Forest fragment. We compared the fate of seeds dispersed by howlers to dispersal by two other frugivores present in the park: capuchin monkeys (Sapajus nigritus) and guans (Penelope superciliaris). Howlers produce clumped defecations that attract dung beetles, which provide secondary dispersal by burying seeds embedded in feces. We expected that seeds dispersed by howlers would have a different fate from those dispersed by capuchins and guans, since their scattered defecations are less attractive to dung beetles. We followed the fate of seeds 3–14 mm in diameter through three processes after seed deposition: secondary dispersal, predation, and seedling emergence. We estimated the probabilities in each step according to the primary disperser and plant species. Dispersal by howlers increased the recruitment of large-seeded plants because of the higher probability of secondary dispersal of the seeds in their feces. Fewer of the seeds dispersed by capuchins or guans were buried, regardless of size, and burial depths were shallower. For 3 mm seeds, the final recruitment probability was similar across frugivores. However, more of the larger seeds reached the seedling stage when dispersed by howlers since they were buried more deeply, which increased their survival without affecting seedling emergence. Reintroductions can thus contribute to restoring ecological processes.
... Dung from captive animals has been used in previous studies (e.g. Raine et al., 2018;Wurmitzer et al., 2017), and it is assumed that small differences in dung odour and quality are unlikely to have consequential effects on the attractiveness of the dung for the beetles, although further investigation is required to confirm this. ...
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Conservation outcomes could be greatly enhanced if strategies addressing anthropogenic land-use change considered the impacts of these changes on entire communities as well as on individual species. Examining how species interactions change across gradients of habitat disturbance allows us to predict the cascading consequences of species extinctions and the response of ecological networks to environmental change. We conducted the first detailed study of changes in a commensalist network of mammals and dung beetles across an environmental disturbance gradient, from primary tropical forest to plantations, which varied in above-ground carbon density (ACD) and mammal communities. Mammal diversity changed only slightly across the gradient, remaining high even in oil palm plantations and fragmented forest. Dung beetle species richness, however, declined in response to lower ACD and was particularly low in plantations and the most disturbed forest sites. Three of the five network metrics (nestedness, network specialization, and functionality) were significantly affected by changes in dung beetle species richness and ACD, but mammal diversity was not an important predictor of network structure. Overall, the interaction networks remained structurally and functionally similar across the gradient, only becoming simplified (i.e., with fewer dung beetle species and fewer interactions) in the most disturbed sites. We suggest that the high diversity of mammals, even in disturbed forests, combined with the generalist feeding patterns of dung beetles, confer resilience to the commensalist dung beetle-mammal networks. This study highlights the importance of protecting logged and fragmented forests to maintain interaction networks and potentially prevent extinction cascades in human-modified systems.
... Community ordination revealed significantly distinct species assemblages between dung types, particularly between nonruminant (elephant and zebra) and ruminant (cattle and giraffe) dung. It is evident that although true specialization is rare in dung breeding beetles, except on non-dung food resources such as carrion or fungus (Larsen et al., 2006;Tshikae et al., 2008), many species show some level of association with a particular dung type (Martin-Piera and Lobo, 1996;Larsen et al., 2006;Frank et al., 2017;Wurmitzer et al., 2017;Tocco et al., 2018). Studies along the aridity gradient of the Botswana Kalahari (mesic northeast-arid southwest) have also shown separation between ruminant (cattle and sheep) and non-ruminant (elephant) dung beetle communities (Tshikae et al., 2013a), and the species found in the current study most closely reflect those of the mesic northeast. ...
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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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Chapter 12 in Dung Beetle Ecology edited by Ilkka Hanski & Yves Cambefort
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Single antennal olfactory cells of the Japanese dung beetle, Geotrupes auratus, which releases food searching behavior in response to cow dung odor, responded well to dung odor and five components of dung specific odorant, namely-2-butanone, phenol, p-cresol, indole and skatole. The impulses were 2-20 mV in height and there were 10-20 impulses per one stimulus of about 3 sec duration. Sensillum cells were classified into two groups based on the type of response to odor components. One was the R-Type I which responded only to 2-butanone (“specialist”), and the other group, the R-Type II, showed responses not only to 2-butanone but also to the other four component odors (“generalist”). Both R-Type I and II cells increased in impulse frequency or number with increase of the concentration of each odorant. It seems that the dung beetles orient toward food through the R-Type I olfactory sensillum cells responding only to 2-butanone which is the most volatile among the components, and that R-Type II cells may contribute to the behavioral Function after arrival at the food. © 1988, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.