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.     

CLEPTOPARASITISM AND DETRITIVORY IN DUNG BEETLE FOSSIL BROOD BALLS FROM PATAGONIA, ARGENTINA

Abstract:  Traces within traces is a new ichnological field that is meant to shed light on significative palaeoecological aspects. Dung beetle fossil brood balls ( Coprinisphaera ispp.), from the Middle Eocene – Lower Miocene Sarmiento Formation of Patagonia, Argentina, show two different trace fossils excavated in its infillings and/or wall that reveal the presence and relationships among different components of past dung communities. Tombownichnus pepei n. isp. is represented by elongated pits, circular to elliptical in cross-section, occurring in the centre or beside ovoid mounds in the internal surface of the Coprinisphaera wall. These traces record the activity of cleptoparasites, such as other dung beetles or flies, whose larvae were probably carried passively with the dung for provisions. Tombownichnus pepei would represent the pupation chambers excavated by full grown larvae in the Coprinisphaera wall after completing their development inside provisioned dung. The other trace fossil, Lazaichnus fistulosus is represented by circular to subcircular borings occurring in Coprinisphaera walls, in connection with an internal gallery in their infillings. Its connection also with meniscate burrows and chambers in the surrounding palaeosol attributable to aestivation chambers of earthworms revealed that these organisms would have been active cleptoparasites or detritivores in dung beetle fossil brood balls.     

Phytolith analysis of Coprinisphaera,unlocking dung beetle behaviour,herbivore diets and palaeoenvironments along the Middle Eocene–Early Miocene of Patagonia

The analysis of the total number of phytoliths, and the absolute frequencies of the different morphotypes, extracted from fossil dung beetle brood balls (Coprinisphaera) from the Middle Eocene–Early Miocene Sarmiento Formation (Patagonia, Argentina), revealed that this trace fossil represents a concentrated locus for phytolith sampling. Particularly, differences found in the total number of phytoliths among parts of that trace fossil and the bearing paleosol, allowed to infer that the infilling represents mostly a sample of the original surrounding soil, whereas in most cases the wall shows a significantly higher number of phytoliths than in the paleosol or infilling. Modern brood balls also revealed that in an environment with high density of grasses, the walls, composed of soil and dung fibres, showed a lower concentration of phytoliths than the soil. In contrast, in other environment with scarce grass coverage, the dung, which had a higher concentration of phytoliths than the soil, added to the wall produced an increase in the number of phytoliths in it. Accordingly, the larger number of phytoliths of the Coprinisphaera wall in comparison with that of the paleosol, would be reflecting the addition of dung fibres to the wall in palaeoenvironments with moderate to poor presence of phytolith-bearing plants. The absence of differences in the total number of phytoliths between the internal and the external layer of the brood ball wall, suggests that the dung fibres would have been uniformly distributed in most of the wall, due to the addition of dung fibres during the brood ball construction by the dung beetle. In contrast, the absence of differences among wall and paleosol or infilling, could be suggesting that no dung fibres were added to construct the wall, that those added had no phytoliths, that the Coprinisphaera involved could had been a brood ball of a necrophagous scarab, or that the soils were richer in phytoltihs than the dung. Those balls that showed evidence of increased numbers of phytoliths in the wall, likely caused by dung fibres added to it, enable the study of diet preferences of the herbivores that produced the dung. Differences found in the phytolith morphotype frequencies among the wall, and the other two samples (infilling and paleosol), allow to infer that some herbivores were more generalists among phytolith-bearing plants feeding on the most abundant grasses and palms, whereas others preferred more rare grasses and dicots.     

Brood Ball-Mediated Transmission of Microbiome Members in the Dung Beetle,Onthophagus taurus (Coleoptera: Scarabaeidae)

Insects feeding on plant sap, blood, and other nutritionally incomplete diets are typically associated with mutualistic bacteria that supplement missing nutrients. Herbivorous mammal dung contains more than 86% cellulose and lacks amino acids essential for insect development and reproduction. Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung. These associations suggest that dung beetles may benefit from mutualistic bacteria that provide nutrients missing from dung. The nesting behaviors of the female parent and the feeding behaviors of the larvae suggest that a microbiome could be vertically transmitted from the parental female to her offspring through the brood ball. Using sterile rearing and a combination of molecular and culture-based techniques, we examine transmission of the microbiome in the bull-headed dung beetle, Onthophagus taurus. Beetles were reared on autoclaved dung and the microbiome was characterized across development. A ~1425 bp region of the 16S rRNA identified Pseudomonadaceae, Enterobacteriaceae, and Comamonadaceae as the most common bacterial families across all life stages and populations, including cultured isolates from the 3^rd instar digestive system. Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus. Scanning electron micrographs of brood balls constructed from sterile dung reveals secretions and microbes only in the chamber the female prepares for the egg. The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber. The transmission of the dung beetle microbiome highlights the maintenance and likely importance of this newly-characterized bacterial community.     

Resource Utilization and Temporal Segregation of Scarabaeinae (Coleoptera,Scarabaeidae) Community in a Caatinga Fragment

We characterized dung beetles food preference and diel activity and examined the way such characteristics may structure a Scarabaeinae community in a dry forest. We sampled a fragment of Arboreal Caatinga in Milagres, Bahia, Brazil, during the dry and wet seasons, using baited pitfall (bovine spleen, human feces, cow dung, and rotten banana). Species were classified by activity (nocturnal and diurnal) and food preference (coprophagous, necrophagous, saprophagous, copro-necrophagous, and generalist). In total, 1,581 individuals belonging to 16 morphospecies were sampled, with six new records for Caatinga. The dung beetles were mainly from generalist and coprophagous species; seven species presented nocturnal activity, and five were diurnal. There was higher species richness during the day and greater abundance during the night. Species composition differences were influenced by functional guilds and beetle size according to temporal segregation. These factors may be related to physiological, morphological, and behavioral differences.     

The volatile organic compounds of introduced and native dung and carrion and their role in dung beetle foraging behaviour

1. The decomposition of biological material produces a plethora of volatile organic compounds (VOCs), which are implicated in the foraging behaviour of coprophagous and necrophagous insects. Dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) have an acute olfactory system used to locate food resources. Accordingly, identification of food resource VOCs potentially used in food location is integral to understanding dung beetle foraging ecology. 2. In this study, volatile emissions from dung and carrion of native and introduced animals in New Zealand were analysed using solid‐phase microextraction (SPME) and gas chromatography‐mass spectrometry (GC‐MS). Volatile profiles were compared via principal component analyses (PCAs) and cluster solutions based on attractiveness using canonical discriminant analysis (CDA). 3. A total of 115 compounds were detected from 21 food types. Statistical analyses showed that dung and carrion volatile profiles clustered according to attractiveness to the dung beetle Saphobius edwardsi, and that different dung types formed distinct clusters and grouped separately from carrion. 4. This study suggests that volatile profiles emitted by food resources used by dung beetles are complex, producing distinct odours, which potentially mediate foraging decisions.     

New Miocene scarabeid and hymenopterous nests and early miocene (santacrucian) paleoenvironments,patagonian Argentina

Three new trace fossils are described from Miocene paleosols of southern Argentina. Celliforma pinturensis, n. ichnosp. and Celliforma rosellii, n. ichnosp. are interpreted as cells of digging bees, possibly Anthophoridae, and Coprinisphaerafrenguellii, n. ichnosp. are brood balls of dung‐beetles. Both burrowing bees and dung‐beetles are common nesters in relatively open areas, confirming previous reconstructions of the paleoenvironment of the Pinturas Formation. A brief review of scarabeid and bee fossil nests from South America is presented, and we propose that constructed nests have a higher preservation potential than excavated nests. This fact explains their more common occurrences as trace fossils in paleosols. A new ethological category, calichnia, is proposed for hymenopterous and coleopterous traces, in which adult individuals make nests exclusively for larvae.     

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.     

Do dung beetle larvae need microbial symbionts from their parents to feed on dung?

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

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The evolution of parental behaviour in Scarabaeinae (Coleoptera, Scarabaeidae): an experimental approach

ABSTRACT.

• 1 Dung beetle lifestyles are reviewed. Most Scarabaeinae lay their eggs in dung masses that are packed into underground chambers, but Coprini and Scarabaeini typically lay their eggs in free-standing brood balls and it is in these tribes that parental care of the brood has evolved.
• 2 Brood balls are constructed by aggregating fragments of dung. This technique is derived from the method of gathering dung at the surface. Larvae developing in brood balls are better protected against dehydration and parasite attack. The repair technique of Scarabaeine larvae preadapts them to life in brood balls.
• 3 Parental care by Copris lunaris depends on appropriate responses by the female to the brood, and it has the selective advantage of protecting the brood against parasites. Preadaptations for parental care in‘non-brooding’Coprini are discussed.
• 4 Variations in the basic Copris nesting behaviour are summarized. Similar variations can occur spontaneously in C.lunaris and can also be released by unusual circumstances.
• 5 C.lunaris females could in principle cooperate but certain factors have prevented this social evolution. The significance of the transient cooperation with the male beetle is discussed.

     

Nest construction, fighting, and larval behaviour in a geotrupine dung beetle, Ceratophyus hoffmannseggi (Coleoptera: Scarabaeidae)

A pair of beetles worked together to make a series of horizontal brood masses by packing dung into underground chambers. An egg was laid in the soil just beyond the tip of each mass. Resident beetles used their horns to resist intruders of either sex. During head-to-head pushing contests in the nest entrance-tunnel, a stable position was adopted where the horns of each opponent thrust harmlessly against the pronotum of the other. The larva prevented collapse of its chamber by building a rigid tube from accurately positioned faecal pellets. Defects in the larval chamber released no obvious repair behaviour and the larva was, therefore, not able to survive in a free-standing brood ball or in the presence of another larva in the same chamber.
It is a pleasure to thank Sr J. de Ferrer (8 Av. F. Franco, Algeciras) for his help and advice.     

Effects of the veterinary antiparasitic drug eprinomectin on dung beetles (Coleoptera: Scarabaeidae), the non-pest fly Neomyia cornicina and pest fly Haematobia irritans (Diptera: Muscidae) in Japan

Effects of the antiparasitic drug eprinomectin were studied in the laboratory and field experiments in Hokkaido, Japan, by pour-on administrations (500 μg/kg) on the pest fly Haematobia irritans (Linnaeus), nontarget coprophagous fly Neomyia cornicina (Fabricius), and the dung beetles Caccobius jessoensis Harold and Liatongus minutus (Motschulsky). Eprinomectin excreted into cattle dung was highest at 3 days post-treatment in both experiments, then it declined rapidly at 7 days and was not detected on or after day 14 post-treatment. In laboratory experiments, pupation and emergence rates of H. irritans and N. cornicina were hampered from 1 to 14 days post-treatment. There were no significant differences in the numbers of brood balls constructed by C. jessoensis in dung from treated and control cattle. Adult emergence rates of C. jessoensis were significantly reduced on days 1 and 3 post-treatment in dung from treated cattle. There were no significant differences in the numbers of brood balls constructed by L. minutus in dung from treated and control cattle, but survival rates of larvae were significantly reduced on days 1 and 3 post-treatment. In field experiments, the numbers of brood balls by L. minutus recovered from beneath dung pats were significantly larger in number in dung from treated cattle, suggesting that adult beetles are attracted to dung pats from treated cattle. Survival rates of larvae in these brood balls of L. minutus were significantly reduced 1 day post-treatment in dung pats from treated cattle, and equivalent levels to the control were restored 7 days post-treatment. The results are discussed in relation to the effects of endectocides on nontarget insects in grazing pastures.     

Attractiveness of dung beetles (Coleoptera: Scarabaeinae) to faeces from native mammals in different trophic guilds

Dung beetles are predominantly coprophagous and use mammalian faeces as their main food resource and for offspring rearing. However, these resources are generally ephemeral and scarce. The objective of this study was to verify the attractiveness to dung beetles of the faeces of nine native mammal species of the Cerrado biome in different trophic guilds. This study was conducted during the rainy season (October 2016 to March 2017) in two sensu stricto areas of the Cerrado in the Brasília National Park (PNB), Federal District, Brazil. Pitfalls containing faeces of nine mammals native to the region were used as bait (from three herbivores, three carnivores and three omnivores) for the collection of dung beetles. We collected 203 individuals and 19 species, and the most abundant species were Uroxys aff. thoracalis, Oxysternon palemo, Coprophanaeus spitzi and Diabroctis mirabilis. The most attractive faecal bait was from the omnivorous Chrysocyon brachyurus (32.67% of the individuals and 13 species). This study reveals variation in the attraction of dung beetles to native mammal dung of the Cerrado, with more abundance in the faeces of omnivores and carnivores and less in the faeces of herbivores. The species composition in the carnivore baits did not differ from that of the omnivore baits. These data indicate that changes in Scarabaeinae assemblages result from changes in mammal species such as those that have occurred in the Cerrado biome with the conversion to cattle production, which in recent years has caused intense fragmentation of habitats, expansion of agricultural and livestock activities and the introduction of exotic species. The mammal C. brachyurus, vulnerable to extinction in Brazil, should be a focus for future research, since its faeces support a great diversity of dung beetles in the Cerrado.     

Development of Copris tripartitus (Coleoptera: Scarabaeidae) in Two Different Rearing Media

ABSTRACT Like many other sub-social insects, Copris tripartitus Waterhouse requires parental care during the development period in the brood balls. Mass-rearing is achieved by using indoor rearing systems and adding more dung after taking away the brood balls containing eggs. Without parental care, larvae are often affected by desiccation, as well as by fungal or sciarid fly intrusion of the brood balls. This study developed a good substitute for brood ball rearing medium. A significantly greater number of progeny survived to adulthood from broods produced by beetles reared on vermiculite medium (90.69±10.98%) than on peat moss medium (44.82±13.92%). Results of the study suggest that to protect the brood balls from desiccation and to produce healthy adults, 15-20% moisture content vermiculite must be used as brood ball rearing medium for most species reared in the laboratory.     

Experimental warming disrupts reproduction and dung burial by a ball‐rolling dung beetle

1. Insects are sensitive to climate change. Consequently, insect‐mediated ecosystem functions and services may be altered by changing climates. 2. Dung beetles provide multiple services by burying manure. Using climate‐controlled chambers, the effects of warming on dung burial and reproduction by the dung beetle Sisyphus rubrus Paschalidis, 1974 were investigated. Sisyphus rubrus break up dung by forming and rolling away balls of manure for burial and egg deposition. 3. To simulate warming in the chambers, 0, 2 or 4 °C offsets were added to field‐recorded, diurnally fluctuating temperatures. We measured dung ball production and burial, egg laying, survival and residence times of beetles. 4. Temperature did not affect the size or number of dung balls produced; however warming reduced dung ball burial by S. rubrus. Because buried balls were more likely to contain eggs, warming could reduce egg laying via a reduction in ball burial. Warming reduced the humidity inside the chambers, and a positive relationship was found between the number of dung balls produced and humidity in two temperature treatments. Temperature did not affect survival, or whether or not a beetle left a chamber. Beetles that did leave the chambers took longer to do so in the warmest treatment. 5. This study demonstrates that climate warming could reduce reproduction and dung burial by S. rubrus, and is an important first step to understanding warming effects on burial services. Future studies should assess warming effects in field situations, both on individual dung beetle species and on aggregate dung burial services.     

Walking on ashes: insect trace fossils from Laetoli indicate poor grass cover associated with early hominin environments

More than 4000 insect trace fossils collected in recent years from Pliocene deposits at Laetoli in northern Tanzania provide new insights on early hominin palaeoenvironments. These trace fossils include: Fictovichnus gobiensis, Coprinisphaera murguiai, C. kheprii, Coprinisphaera ispp., Quirogaichnus isp., Teisseirei linguatus isp. nov., Celliforma ritchiei isp. nov., C. spirifer, C. germanica, C. cfr. curvata, Celliforma ispp., Rosellichnus isp., Vondrichnus planoglobus, Laetolichnus kwekai igen. et isp. nov. and Krausichnidae indet. They reveal that at least one species of moth, three dung beetles and five other coleopterans, nine taxa of solitary bees, and an indeterminate number of taxa of termites inhabited the Lower Laetolil environments. The Upper Laetolil environments, which have yielded a rich diversity of vertebrate fossils, including the early hominin Australopithecus afarensis and its putative footprints, supported several taxa of termites, one dung beetle, five other coleopterans, and eleven taxa of bees. The Upper Ndolanya environments, which have yielded the hominin Paranthropus aethiopicus, record four taxa of dung beetles, four other coleopterans, and two taxa of bees. The record of larval mortality and lack of intruder activity, revealed by the absence of emergence and intruder traces, may be associated with the anoxic/hypoxic conditions caused by the instantaneous burial of soils under thick volcanic ashes. The record of the Celliforma Ichnofacies in the Upper Laetolil environments indicates the dominance of shrubland to woodland with limited grass cover. This is supported also by the absence of Coprinisphaera, which suggests a scarcity of fresh grasses and a low abundance of large mammal grazers.     

Male Participation in Nest Building in the Dung Beetle Scarabaeus catenatus (Coleoptera: Scarabaeidae): Mating Effort Versus Paternal Effort

The dung beetle, Scarabaeus catenatus, shows not only the rolling but also the tunneling tactic for nest building with bisexual cooperation. Sex roles, however, differed between the tactics. In rolling, the male took the initiative like that of ball-roller species: he rolled a dung ball away and buried it. In tunneling, in contrast, the male usually had a secondary role like that of tunnelers: he was less active in burrow excavation and provisioning. Regardless of the tactics, male participation did not increase female reproductive output measured by the number or size of brood balls in the field, but seemed to function as mate guarding against conspecific males. This suggests that, in both tactics, the male S. catenatus invests primarily in mating effort compared with paternal effort. The relative importance of mating effort in male participation seems to hold true in other dung beetles, irrespective of whether they are ball-roller or tunneler species. In addition, the male mating strategy of S. catenatus is compared with that of other ball-rollers.     

Nesting strategies and disease risk in necrophagous beetles

While the effects of carcass decomposition on microorganisms have been demonstrated in recent years, little is known of how this impacts necrophagous insects. A common assumption is that insects that exploit carcasses are exposed to a high density of potentially harmful microorganisms, but no field data have so far validated this. Necrophagous beetles such as the Scarabaeinae have complex nesting behaviors with elaborate parental care. So here, we begin to explore whether this conjunction of life history and nesting behavior represents an adaptive response to the threat posed by microbes in these environments, mainly by entomopathogens. We evaluated the density and distribution of fungi and bacteria from soil near the carcasses, and their ability to infect and kill insects that are in contact with this soil during the decomposition process. Our data showed an increase in the density and activity of opportunistic or facultative pathogens during the apex of decomposition, when there is a predominance of necrophagous insects. Meanwhile, the survivorship of bait insects decreased when in contact with soil from this period of decomposition, indicating a potential risk of infection. However, the density and activity of these microorganisms decreased with distance from the carcass, mainly with depth, which would benefit tunneller beetles in particular. We have thus provided the first field data to show that necrophagous insects are indeed exposed to high densities of potentially harmful microorganisms. Furthermore, we propose that some parental care strategies may have arisen not only as a response to competition, but also as adaptations that reduce the risks of disease. Although we have focused on carrion feeders, we suggest that the same occurs with coprophagous beetles, as both carrion and dung are nutrient‐rich resources.     

Brood ball construction by the non-brooding Coprini Sulcophanaeus carnifex and Dichotomius torulosus (Coleoptera, Scarabaeidae)

ABSTRACT.

• 1 Feeding burrows made by S.carnifex and D.torulosus adults consisted of tunnels filled with sausage-shaped masses of dung. Brood balls were made by taking fragments of dung from an adjacent feeding burrow and aggregating them into a small sphere which was gradually enlarged and then coated with soil.
• 2 S.carnifex adult females showed no response to their own eggs (unlike Copris lunaris: Klemperer, H.G. (1982) Ecological Erltonzology, 7, 155–167). S.carnifex larvae made and maintained an air channel to the upper pole of the ball and they are in this respect preadapted to receive parental care.
• 3 Compared with a brood mass, a brood ball was less likely to be attacked by Meptoparasitic larvae. The soil coat retarded drying of the brood ball by increasing the total mass of moisturecontaining material.