Experimental warming alters the relative survival and emigration of two dung beetle species from an Australian dung pat community

To preserve insect‐mediated ecosystem services under ongoing climate change, it is necessary to first understand the impact that warming will have on the insects that provide or mediate these services. Furthermore, because responses of a species may be modified by interactions with competitors, it is informative to examine warming effects on organisms and service provision under competition. Dung beetles provide numerous services to agriculture by burying the manure of other animals. To understand the potential impacts of climate warming on ecosystem service provision, we exposed two dung beetle species (Sisyphus rubrus and Euoniticellus fulvus (Coleoptera: Scarabaeidae)), occurring together in the same experimental pats, to warming and measured reproduction (dung ball production and burial, brood production, and egg laying), pat departure behaviour and survival of both species. These two species are likely competitors in pastures in northern New South Wales. To simulate climate warming, we used custom‐built chambers to add offsets (+0, +2 or +4°C) to field recorded, diurnally fluctuating baseline temperatures. There was no direct effect of increased temperature on any measured trait in either species. We did find however that the relative survival of the two species depended on temperature; S. rubrus had a higher probability (resulting in greater odds) of surviving than E. fulvus in the +0 and +4°C offset chambers, but not in the +2°C offset chambers. Likewise, the relative likelihood of the different species leaving a dung pat was temperature dependent; in the +2°C offset chambers, E. fulvus were more likely to leave than S. rubrus, but not in the +0 and +4°C offsets chambers. Our results highlight that it may be important for future studies to consider warming effects on relative survival and emigration because such effects could potentially lead to changes in dung beetle species composition.     

Beyond Coprinisphaera: fossil nests of dung beetles

Forty‐two remains of fossil nests of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae), which were recorded in four formations of the Cenozoic of South America, are described herein for the first time. Most of them are represented by nesting chambers containing a fossil brood ball (Coprinisphaera). However, in the most remarkable cases, parts of the burrows constructed by the parents and/or the vertical emergence burrows constructed by the offspring are preserved too. The preservation of the dung beetle nests is very unusual but more recurrent in younger formations probably because of the short‐term action of the diagenetic processes. Considering that the construction of brood balls always involves the construction of nests, the ichnotaxonomical proposal is that the remains of fossil nests should be considered as ‘structures associated with Coprinisphaera’ and added to the diagnosis to avoid the proliferation of names. The study of the fossil nests provides new palaeoetological inferences for dung beetles, such as the Nesting Pattern of the trace makers of Coprinisphaera tonnii and Coprinisphaera akatanka, and how phylogenetically related were they with the extant necrophagous species of the genera Coprophanaeus and Canthon, respectively. Additionally, the fossil evidence suggests that simple nests of dung beetles predate compound nests.     

Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae

Vertebrate dung is central to the dung beetle life cycle, constituting food for adults and a protective and nutritive refuge for their offspring. Adult dung beetles have soft mandibles and feed primarily on nutritionally rich dung particles, while larvae have sclerotized mandibles and consume coarser dung particles with a higher C/N ratio. Here, using the dung beetles Euoniticellus intermedius and E. triangulatus, we show that these morphological adaptations in mandibular structure are also correlated with differences in basic gut structure and gut bacterial communities between dung beetle life stages. Metagenome functional predictions based on 16S rDNA characterization further indicated that larval gut communities are enriched in genes involved in cellulose degradation and nitrogen fixation compared to adult guts. Larval gut communities are more similar to female gut communities than they are to those of males, and bacteria present in maternally provisioned brood balls and maternal ‘gifts’ (secretions deposited in the brood ball along with the egg) are also more similar to larval gut communities than to those of males. Maternal secretions and maternally provisioned brood balls, as well as dung, were important factors shaping the larval gut community. Differences between gut microbiota in the adults and larvae are likely to contribute to differences in nutrient assimilation from ingested dung at different life history stages.     

Brood ball size but not egg size correlates with maternal size in a dung beetle,Onthophagus atripennis

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Newly released non‐native dung beetle species provide enhanced ecosystem services in New Zealand pastures

1. Whether the release of non‐native insect species benefits or harms ecosystem services has been the subject of debate. In New Zealand, the release of new non‐native dung beetle species was intended to enhance ecosystem services but concerns were raised over possible negative effects. 2. Field cage trials used three newly released dung beetle species to investigate two concerns: that soil disturbance from dung beetle activity increases soil losses in runoff after rainfall; and that dung burial increases survival of infective parasitic nematodes on pasture. 3. Three treatments – dung + beetles, dung‐only, and controls (without dung or beetles) – were applied on each of three soil types with different permeability: sandy loam, clay loam, and compacted clay. 4. Dung beetle activity resulted in significant reductions of 49% and 81% in mean surface runoff volume, depending on simulated rainfall intensity. Amounts of sediment in the runoff did not change under an extreme rainfall simulation, but in a less extreme rainfall simulation the presence of dung beetles resulted in a 97% reduction in mean sediment amount in runoff. 5. The numbers of infective third‐stage nematode larvae recovered from foliage varied considerably between soil types and through time; however, dung beetle activity reduced overall mean nematode numbers on grass around the dung pats by 71%. 6. This study adds to global evidence that dung beetles can improve agricultural ecosystem services by providing data on services that have rarely been investigated: reduced runoff/soil losses through increased soil porosity, and reductions in parasitic nematodes.     

Asymmetric competition in cattle dung between two species of Onthophagus dung beetle and the bush fly, Musca vetustissima

Abstract.

• 1 Competition in cattle dung pads between two dung beetles, Onthophagus ferox Harold and Onthophagus binodis Thunberg, and the bush fly, Musca vetustissima Walker, was investigated in laboratory experiments, to determine why spring fly abundance in the field did not fall following the introduction of O. binodis.
• 2 At low beetle densities, the number of eggs laid by each species was reduced by the second species. A similar amount of dung was buried by each species alone or by both together.
• 3 At high beetle densities O. binodis egg production was substantially affected by each additional O.ferox, but O.ferox egg production was not affected by each additional O.binodis. Asymmetric competition occurred because O.ferox buried more dung than O.binodis, and a greater proportion in day 1 (pre-emptive dung burial).
• 4 O.ferox caused greater M. vetustissima egg-puparia mortality than O. binodis. Mortality mostly occurred in young M. vetustissima larvae less than 1 day old. Total egg-puparia fly mortality was correlated better with the dung buried on day 1 than dung buried on day 8 (pre-emptive dung burial). O.binodis did not add to fly mortality by O.ferox at high densities because of asymmetric competition between the beetles.

     

Bearing selection in ball-rolling dung beetles: is it constant?

Ball rolling in dung beetles is thought to have evolved as a means to escape intense inter- and intra-specific competition at the dung pile. Accordingly, dung beetles typically roll along a straight-line path away from the pile, this being the most effective escape strategy for transporting dung to a suitable burial site. In this study, we investigate how individual diurnal dung beetles, Scarabaeus (Kheper) nigroaeneus, select the compass bearing of their straight-line rolls. In particular, we examine whether roll bearings are constant with respect to geographic cues, celestial cues, or other environmental cues (such as wind direction). Our results reveal that the roll bearings taken by individual beetles are not constant with respect to geographic or celestial references. Environmental cues appear to have some influence over bearing selection, although the relationship is not strong. Furthermore, the variance in roll bearing that we observe is not affected by the presence or absence of other beetles. Thus, rather than being constant for individual beetles, bearing selection varies each time a beetle makes a ball and rolls it away from the dung pile. This strategy allows beetles to make an efficient escape from the dung pile while minimizing the chance of encountering competition.     

Effect of dung burial by the dung beetle Bubas bison on numbers and viability of Cryptosporidium oocysts in cattle dung

Cryptosporidium oocysts were inoculated into fresh dung (∼1.2 × 10⁴ oocysts per gram wet weight) and fed to dung beetles to assess the effect of dung burial by the dung beetle Bubas bison on the distribution of the oocysts in small cores of soil in the laboratory. The experiment consisted of five replicates of each of two treatments; controls (dung but no dung beetles) and the experimental treatment (inoculated dung and seven pairs of dung beetles). After 5 days, when approximately 90% of the dung was buried, the surface and buried dung was recovered and subsampled. The oocysts in the subsamples were recovered and enumerated using qPCR. Oocyst viability was evaluated using an assay based on the exclusion or inclusion of two fluorogenic vital dyes, 4′,6-diamidino-2-phenylindole (DAPI) and propidium iodide (PI). Results revealed that overall 13.7% of oocysts remained on the surface and 86.3% of oocysts were buried. The viability of oocysts in buried dung was only 10% compared to oocysts the surface dung (58%). Therefore, widespread dung burial by B. bison during the winter months could substantially reduce the numbers of Cryptosporidium oocysts available to be washed into waterways following winter rains.     

The earliest burst of necrophagous dung beetles in South America revealed by the Cenozoic record of Coprinisphaera

New ichnological, sedimentological and palaeobotanical information from a Miocene palaeosol succession from Patagonia bearing abundant fossil brood balls of dung beetles (Coprinisphaera) allow inferring novel aspects of the evolutionary history, biology and feeding habits of Scarabaeinae, along with the palaeoenvironmental and palaeoclimatic conditions in which they nested. Coprinisphaera tonnii and Coprinisphaera akatanka, both attributed to necrophagous dung beetles, represent 40.2% of the specimens. Considering their scarce or null record in older Cenozoic units from South America, these high values reveal that the first burst of necrophagous Scarabaeinae took place during the Miocene. Some Coprinisphaera preserve characters that indicate the developmental stage of the ball occupant and the adult emergence success. Both ichnospecies show the egg chamber isolated from the provision chamber, which was associated with a higher preference of cleptoparasites for necrophagous balls. The comparison among the abundance of traces of nest intruders in Coprinisphaera attributed both to necrophagous and to coprophagous beetles from different units of South America indicates that the presence of such intruders would be independent of the nature of the organic matter contained within the balls. Phytolith analyses performed in Coprinisphaera and extant necrophagous and coprophagous balls indicate that the comparison between the relative abundance of phytoliths in the wall of the brood ball, their infilling and the bearing palaeosol is a useful tool for inferring the feeding behaviour of the trace makers and support the attribution of Coprinisphaera tonnii and Coprinisphaera akatanka to necrophagous Scarabaeinae. Sedimentary and palaeosol analyses indicate that the beetles would have nested in well-drained soils showing mollic-like features, in grass-dominated habitats, under a seasonal sub-humid, temperate–warm climate.     

Generalist dung attraction response in a New Zealand dung beetle that evolved with an absence of mammalian herbivores

1. Dung beetles (Scarabaeidae: Scarabaeinae) are integral parts of many ecosystems because of their role in decomposition of dung; particularly mammal dung, which forms the diet of both larvae and adults. 2. New Zealand dung beetles are unusual as they are flightless and evolved on islands with a highly depauperate mammal fauna and thus without the usual dung resource used by dung beetles elsewhere. The diet of New Zealand dung beetles is unknown. 3. We hypothesised (1) that the endemic dung beetle Saphobius edwardsi would be attracted to a broad range of food types, and (2) that S. edwardsi would be able to survive and reproduce on a range of dung types and puriri (Vitex lucens) humus. 4. Laboratory choice tests identified that S. edwardsi was attracted to a range of mammal, bird, invertebrate, and reptile dung types, but not to non‐dung food sources. Five‐month no‐choice tests found that beetle survival rates were lower for beetles fed with humus compared with those fed on mammal, bird, or invertebrate dung. None of the beetles reproduced. 5. This study suggests S. edwardsi have a strong preference for dung, and are likely to be broad dung generalists in their feeding behaviour.     

Oviposition of the dung beetle Aphodius ater in relation to the abundance of yellow dungfly larvae (Scatophaga stercoraria)

1. The dung beetle Aphodius ater and the yellow dungfly Scatophaga stercoraria are temporally co-occurring species in sheep dung, which they use for reproduction and nutrition ( A. ater ) or for reproduction only ( S. stercoraria ) during the spring in northern Germany. Scatophaga stercoraria uses fresh sheep dung pellets a few hours old for oviposition, whereas A. ater lays eggs into 2–10-day-old pellets. In the present study, the egg laying behaviour of A. ater in sheep dung in relation to the presence of larvae of S. stercoraria was investigated experimentally.
2. Choice experiments, based on examining the egg laying behaviour of beetles in 2- and 4-day-old pellets with and without high and low densities of fly larvae, showed the following. In 2-day-old pellets, the beetles did not distinguish between pellets without fly larvae or with fly larvae at low larval density but avoided laying eggs into pellets with a high larval density. In 4-day-old pellets, the beetles always preferred to lay their eggs into pellets without fly larvae, regardless of larval density.
3. The influence of different densities of larvae of S. stercoraria on dung depletion was examined by measuring the dry weight, organic matter content and organic nitrogen content of the remaining dung after larval development. The presence of the larvae led to a reduction in all three parameters.
4. The beetles' behaviour of laying eggs into older pellets, and their awareness of the presence of high densities of fly larvae, enables them to avoid egg laying into pellets that will have been depleted by fly larvae before the beetle larvae have finished their development.     

Habitat and weather affect reproduction and size of the dung beetle Aphodius fossor

1. The influence of sun exposure and moisture on reproduction and size of a north temperate dung beetle Aphodius fossor was investigated. Adult beetles were added to cow pats that were either shaded or exposed and treated with different watering regimes. 2. After 26 days, more eggs and larvae were recovered from shaded and wetter pats than from exposed and drier pats. 3. At the end of the experiment, more beetles had developed in shaded and wetter pats, and these beetles were larger than those from exposed and drier pats. 4. There was no between‐treatment difference in the ratio between adults in final sampling and larvae in first sampling. 5. It was concluded that exposure and moisture can influence both reproduction and size of A. fossor. It is suggested that weather may be a factor regulating reproduction in Aphodius not only through heat‐ or drought‐induced mortality, as suggested earlier, but also by limiting the time available for egg laying. Further studies are needed to clarify this suggestion.     

Evidence that sex‐specific signals may support mate finding and limit aggregation in the dung beetle Aphodius fossor

1. In temperate climates, dung is often colonised by several species of endocoprid (dwelling) dung beetles which use pats for feeding, shelter, and reproduction. 2. Endocoprid beetles aggregate even when offered patches (dung pats) of consistent age, size, and origin, suggesting that beetles themselves might influence the attractiveness of patches to members of their own species. Both pheromones, and physical changes to the structure of dung pats caused by colonising beetles have been suggested as mechanisms facilitating intraspecific aggregation, but neither of these hypotheses have been empirically tested. 3. Using a common European dung beetle (Aphodius fossor L.), we conducted a simple choice experiment designed to test whether (i) earlier colonisation by conspecifics could alter dung attractiveness and (ii) whether attraction was influenced by sex‐specific signals. 4. We found that female beetles are repelled by dung colonised by conspecific females and are attracted to dung colonised by conspecific males. Male beetles show no evidence of attraction or repellence for dung colonised by either sex. Neither in females nor males was uncolonised dung found to be significantly more or less attractive than predicted by non‐preference. 5. Our results suggest that for A. fossor male‐produced signals may support mate finding in patchy environments, and that female‐produced signals may serve to discourage subsequent colonisation by additional females.     

Fire? They don't give a dung! The resilience of dung beetles to fire in a tropical savanna

1. Disturbance is a strong driver of community assembly and fire has long been recognised as one of the main disturbances of terrestrial ecosystems. This study tested the resilience of dung beetles to fire events in campos rupestres, which is a tropical savanna ecosystem that evolved under a frequent fire regime, by assessing the resistance and recovery of their communities. 2. Dung beetles were sampled before and after a fire event and the effect of fire on dung beetle richness, abundance, mean community biomass and composition was tested. The effects of time since last fire and fire frequency on the community were also tested. 3. No effect of fire occurrence, time since last fire and fire frequency on any community variable was found. 4. Some non‐mutually exclusive mechanisms promoting the resistance and recovery of dung beetles in campos rupestres could be acting in synergy. One potential mechanism is the mismatched seasonality between fire events and dung beetle occurrence, as fires occur during the dry season and dung beetles are present above ground during the rainy season. Furthermore, dung beetles are insects that remain buried during most of their lifetime, which could protect individuals from being burned. Another potential mechanism is the replacement of species in burned areas by the movement of individuals from unburned areas, attracted by resources and/or by metacommunity dynamics. 5. It is concluded that in this ‘fire‐dependent’ ecosystem, dung beetle communities are resilient to fire and seem not to be structured by this disturbance.     

Contest dynamics for food and reproductive resources are defined by health condition in a dung beetle

Male dung beetles compete to obtain food and females, and early resource recognition and appropriation increase the probability of mating. The outcome of such encounters is expected to be defined by self‐ and the opponent’s health condition. In this study, we analyzed the effect of body condition and immune defense on the contest dynamics between males that rolled a food ball with a partner female (owner males) and intruder males of dung beetle Canthon cyanellus. Body condition was measured as body size, body dry mass, lipid mass, and muscle mass; immune defense was estimated via phenoloxidase activity. Owner males with higher lipid mass contacted the food ball significantly earlier than owner males with lower lipid mass. Individuals with lower phenoloxidase activity started to roll food balls earlier than individuals with higher phenoloxidase activity. Owner males that had higher body dry mass, compared to female partners, began to roll the food ball significantly earlier than male–female pairs with lower differences in dry mass. Heavier males won significantly more contests than lighter males. Our results suggest that the health condition is a key factor related to the dynamics and outcome of male–male contests for resources and females in C. cyanellus. Consequently, differences in individual condition are main determinants of contest outcomes in dung beetles.     

Visual cues used by ball-rolling dung beetles for orientation

Ball rolling by dung beetles is considered to be a derived behaviour that evolved under pressure for space, and from competitors at the dung pat. Straight-line orientation away from the pat using a celestial cue should be the most successful rolling strategy to move dung to an unknown burial site. We tested this hypothesis in the field and the laboratory by presenting five species of ball-rolling beetles with different orientation tasks, involving reaction to obstacles as well as to reflected sunlight and artificial light sources. Beetles were found to consistently orientate along a chosen route, usually in the direction of the sun. Beetles rolling dung balls successfully negotiated barriers and returned to the original path as did beetles falling from ramps, or rotated about a fixed point while rolling a ball. The sun was found to be the main orientation cue, which could be substituted by reflected or artificial light. However, beetles reoriented themselves less accurately in response to lights in the laboratory, than they did to the reflected sun in the field. It is probable that phototactic orientation using the sun, which is widespread amongst arthropods, has been incorporated in the straight-line foraging behaviour that has evolved in ball-rolling dung beetles.     

Patterns of alimentary resource use by dung beetles in introduced Brazilian pastures: Cattle versus sheep dung

Dung beetles (Coleoptera: Scarabaeidae) perform essential ecological functions in pastures, such as dung removal, nutrient recycling and parasite control. However, the patterns of alimentary use by dung beetles in introduced Brazilian pastures are poorly known. Here, we compared dung beetle species richness, abundance and species composition in cattle and sheep dung, and identified the dung beetle species preference by each dung type. In January 2019, dung beetles were sampled with pitfall traps baited with cattle and sheep dung in 12 introduced pastures (Urochloa spp.), in Aquidauana, Mato Grosso do Sul, Brazil. A total of 592 individuals belonging to 14 species of dung beetles were collected. Of the 14 species sampled, nine were recorded in both dung types, five were found exclusively in sheep dung and no species was exclusive to cattle dung. Species richness and abundance were higher in sheep dung. Species composition was different between the dung types. Dichotomius bos (Blanchard), Genieridium bidens (Balthasar), Onthophagus aeneus Blanchard and Trichillum externepunctatum Preudhomme de Borre were associated with sheep dung. Our results provide evidence that sheep dung is more attractive to dung beetles with a distinct community species between the two dung types, although the studied pastures have never been used before for sheep breeding. Thus, our data shows that the introduction of a new alimentary resource (e.g. sheep dung) can be an important strategy to help to obtain a more diverse dung beetle assemblage in introduced Brazilian pastures.     

Space-for-time substitution reveals a hump-shaped distribution of dung beetles

Unraveling how climate change impacts the diversity and distribution patterns of organisms is a major concern in ecology, especially with climate-sensitive species, such as dung beetles. Often found in warmer weather conditions, beetles are used as bio-indicators of environmental conditions. By using an altitudinal gradient as a proxy for climate change (i.e., space-for-time substitution), we assessed how changes in climatic variables, such as temperature and precipitation, impact patterns of dung beetle diversity and distribution in the Peruvian Andes. We recorded dung beetle diversity using three different types of baits, feces, carrion, and fruits, distributed in 18 pitfall traps in five different altitudinal sites (from 900 to 2500 m, 400 m apart from each other) in the rainy and dry season. We found that (i) dung beetle richness and abundance were influenced by the climate gradient, (ii) seasonality influenced beetle richness, which was high in the wet season, but did not influence abundance, (iii) dung beetle richness and abundance fit to a hump-shaped distribution pattern along the altitudinal gradient, and (iv) species richness is the beta-diversity component that best describes the composition of dung beetle species along the altitudinal gradient. Our data show that the distribution and diversity of dung beetles are different at larger scales, with different patterns resulting from the response of species to both abiotic and biotic factors.     

Down‐sizing of dung beetle assemblages over the last 53 000 years is consistent with a dominant effect of megafauna losses

The ongoing down‐sizing of the global mammal communities is assumed to have subsequent effects on mutualistic species communities. Dung beetles co‐evolved with large‐sized animals since millennia and depend on the megafauna feces of an appropriate size. Mammal community down‐sizing as a result of past and ongoing megafauna losses is therefore likely to result in a down‐sizing of dung beetle communities. However, empirical evidence for this co‐down‐sizing is lacking especially on larger spatial scales and over extended periods of time. Here, we show a significant down‐sizing of European dung beetle assemblages over the last ~53 000 years by relating Quaternary fossil records with trait information on body size of beetles. This significant down‐sizing of dung beetle communities was thereby not linear, but characterized by a weak decrease until the early Holocene but a strong acceleration in the recent pre‐history, from 6–7000 years BP onwards. This acceleration of down‐sizing coincides with the completion of the Quaternary megafauna extinction and the start of major shifts in human agricultural land‐use. In contrast, assemblage mean body size of non‐coprophagous scarabids as well as ground beetles – two groups of beetles with no or weak relations to megafauna – was observed to increase towards the present with an acceleration of body size increase coinciding with the onset of late‐glacial warming (14 200 years BP). In summary, the observed late‐Quaternary down‐sizing of European dung beetle communities is consistent with an effect of pre‐historic megafauna losses, and not with the coincident general warming. Ongoing down‐sizing of mammal communities is therefore likely to result in further down‐sizing of dung beetle assemblages, with potential effects on their important role for nutrient cycling and secondary seed dispersal in natural and extensive agro‐ecosystems. Future nature management initiatives could halt or even reverse this functional diversity loss via effective protection or restoration of megafauna communities.     

A functional classification for analysis of the structure of dung beetle assemblages

Abstract. 1. Regional scarabaeid dung beetle assemblages in southern Africa may contain over 100 species, ranging in live weight from 10 mg to 10 g. These show a wide variety of dung-use and reproductive strategies.
2. To facilitate analysis of these diverse assemblages, a system of classification analogous to guilds is proposed. Scarabaeid dung beetle species are allocated to one of seven functional groups (FGs) according to the way they use and disrupt dung. Each group therefore contains a set of species which are functional analogues of each other. This classification provides a conceptual framework within which to analyse the structure of dung beetle assemblages and the interactions between dung beetles and other dung-breeding species such as coprophagous flies.
3. There is a clear hierarchy of functional groups in their ability to compete for dung. Competitively dominant groups such as the large ball rollers (FG I) and fast-burying tunnellers (FG III) are mostly large, aggressive beetles which rapidly remove dung from the pad. The smaller ball rollers (FG II) are also effective competitors for dung. Subordinate groups are those which bury dung slowly over many days (FG IV and V) and those which breed inside the pad (FG VII, endocoprids). Kleptocoprids (FG VI) breed in dung buried by other beetles and so are not part of the hierarchy.
4. The use of this classification is illustrated by reference to three contrasting assemblages of dung beetles in a summer rainfall region of southern Africa. The potential of these beetles for biological control of dung-breeding flies is discussed.