Impacts of warmer temperatures on secondary seed dispersal by Phanaeus vindex dung beetles (Scarabaeinae).

Anthropogenic changes are often studied in isolation but may interact to affect biodiversity. For example, climate change could exacerbate the impacts of biological invasions if climate change differentially affects invasive and native species. Behavioural plasticity may mitigate some of the impacts of climate change, but species vary in their degree of behavioural plasticity. In particular, invasive species may have greater behavioural plasticity than native species since plasticity helps invasive species establish and spread in new environments. This plasticity could make invasives better able to cope with climate change. Here our goal was to examine whether reproductive behaviours and behavioural plasticity vary between an introduced and a native Onthophagus dung beetle species in response to warming temperatures and how differences in behaviour influence offspring survival. Using a repeated measures design, we exposed small colonies of introduced O. taurus and native O. hecate to three temperature treatments, including a control, low warming and high warming treatment, and then measured reproductive behaviours, including the number, size and burial depth of brood balls. We reared offspring in their brood balls in developmental temperatures that matched those of the brood ball burial depth to quantify survival. We found that the introduced O. taurus produced more brood balls and larger brood balls, and buried brood balls deeper than the native O. hecate in all treatments. However, the two species did not vary in the degree of behavioural plasticity in response to warming. Differences in reproductive behaviours did affect survival such that warming temperatures had a greater effect on survival of offspring of native O. hecate compared to introduced O. taurus. Overall, our results suggest that differences in behaviour between native and introduced species are one mechanism through which climate change may exacerbate negative impacts of biological invasions.

Temperature profoundly impacts insect development, but plasticity of reproductive behaviours may mediate the impacts of temperature change on earlier life stages. Few studies have examined the potential for adult behavioural plasticity to buffer offspring from the warmer, more variable temperatures associated with climate change. We used a field manipulation to examine whether the dung beetle Phanaeus vindex alters breeding behaviours in response to temperature changes and whether behavioural shifts protect offspring from temperature changes. Dung beetles lay eggs inside brood balls made of dung that are buried underground. Brood ball depth impacts the temperatures offspring experience with consequences for development. We placed adult females in either control or greenhouse treatments that simultaneously increased temperature mean and variance. We found that females in greenhouse treatments produced more brood balls that were smaller and buried deeper than controls, suggesting brood ball number or burial depth may come at a cost to brood ball size, which can impact offspring nutrition. Despite being buried deeper, brood balls from the greenhouse treatment experienced warmer mean temperatures but similar amplitudes of temperature fluctuation relative to controls. Our findings suggest adult behaviours may partially buffer developing offspring from temperature changes.

The dung beetle primarily feeds on the feces of herbivorous animals and play a crucial role in ecological processes like material cycles and soil improvement. This study aims to explore the diversity and composition of the gut microbiota of Catharsius molossus (a renowned dung beetle originating from China and introduced to multiple countries for its ecological value) and exploring whether these gut microbes are transmitted vertically across generations. Using 16S rRNA and ITS rRNA gene sequencing techniques, we described the diversity and composition of gut microbes in C. molossus from different localities and different developmental stages (Egg, young larvae and old larvae). We discovered that the diversity of gut microbiota of dung beetles varied obviously among different geographical localities and different developmental stages, and we also discussed the potential influencing factors. Interestingly, the microbial community structure within the brood balls is more similar to male dung beetle than to that of females, which is consistent with the observation that the brood ball is constructed by the male dung beetle, with the female laying egg in it at the final step. This unique breeding method facilitates offspring in inheriting microbial communities from both the mother and the father. Initially, the larvae's gut microbiota closely mirrors that of the parental gift in these brood balls. As larvae grow, significant changes occur in their gut microbiota, including an increase in symbiotic bacteria like Lactococcus and Enterococcus. Analysis of the gut bacteria of adult dung beetles across various localities and different developmental stages identified nine core genera in adults, contributing to 67.80% of the total microbial abundance, and 11 core genera in beetles at different developmental stages, accounting for 49.13% of the total. Notably, seven genera were common between these two core groups. Our results suggest that Parental gifts can play a role in the vertical transmission of microbes, and the abundance of probiotics increases with larval development, supporting the hypothesis that "larval feeding behavior occurs in two stages: larvae first feed on parental gifts to acquire necessary microbes, then enrich symbiotic microbiota through consuming their own feces."

Equal numbers of newly emerged male and female Onthophagus binodis Thunberg were placed at densities from 2–100 beetles on one‐litre pads of cattle dung. After one week the number of brood balls produced was counted and the volume of dung dispersed (buried and shredded) visually assessed. The surviving beetles from each box were then placed on another pad, and the process repeated until all beetles were dead. Beetle survival was not influenced by initial beetle density and fell linearly with time (P < 0.001). Brood ball production/female/week did not appear to be influenced by beetle age and could be predicted from current beetle density Y = 15.03e−0.045X, R2 = 0.42. Dung dispersal increased with increasing density up to about 35 beetles/pad, above which the proportion dispersed plateaued at about 90%. Dung burial, estimated from the number of brood balls produced/week, was on average greatest (450 ml) with 20–30 beetles/pad. The effect of density on production of brood balls was inferred to reflect the frequency of contact between adults in the pad.RÉSUMÉEffets de la densité de la population sur la reproduction et la dispersion des bouses chez Onthophagus binodis au laboratoireL'examen au laboratoire a porté sur la relation entre le nombre d'Onthophagus binodis Thunberg et le nombre de pelotes pour l'alimentation larvaire produite par femelle dans des galettes de un litre de bouse de vache. Un nombre déterminé d'insectes a été placé sur la bouse et le nombre de pelotes dénombré chaque semaine, les adultes survivants ont été dénombrés et placés sur une nouvelle galette de bouse. Cette opération a été répétée chaque semaine jusqu'à ce que tous les insectes du lot aient été morts.La survie a diminué linéairement avec le temps sans avoir été influencée par la densité d'origine (de 2 à 100 insectes par paquet). Après une période d'une semaine précédant la reproduction, une relation non linéaire inverse entre la production de pelotes par femelle et le nombre d'insectes présents a pu être observée. Les régressions linéaires de données transformées (logarithmes de X et Y) ont été comparées pour 14 cohortes d'insectes âgés de 2 à 19 semaines. Pour des raisons pratiques, les régressions sont semblables pour les insectes de tous âges. Une fonction exponentielle négative a été utilisée pour relier la production de pelotes (Y) à la densité des insectes (X):Y = 15,03e−0.45x avec R2 = 0,42 et F = 67,53 pour 2 et 188 df (P < 0,001).La quantité de bouse travaillée à chaque densité a été calculée à partir du nombre de pelotes produites par semaine et le volume de galette utilisé pour faire chaque pelote. La quantité de bouse travaillée culmine à 450 ml quand 25 à 35 insectes sont dans la galette. Aux densités supérieures à 35 insectes, la plus grande partie de la galette est dispersée, mais l'essentiel de celle‐ci est fragmentée et non travaillée. Une courbe de Michaelis et Mantus a été employée pour décrire la relation entre le volume de bouse dispersée (axe Y) et le nombre d'insectes (axe X): Y = 89,29X/1 + 0,084X avec R2 = 0,64, F = 145,23 pour 2 et 162 df (P < 0,001).La densité d' O. binodis n'a influencé significativement, ni la production de pelotes complètes (6% étaient inachevées), ni la proportion de pelotes qui contenaient des chambres d'incubation d'oeufs (86%, n = 663). Ainsi les réactions à la diversité se produisent avant le début de la fabrication de la pelote, ce qui permet de déduire qu'elles reflètent la fréquence des contacts entre adultes dans la galette.

The dung beetle Copris tripartitus Waterhouse (Coleoptera: Scarabaeidae) is a coprophagous insect that lives in and feeds primarily on the feces of mammalian herbivores and is known to protect their offspring from the pathogen-rich environment by performing parental care for brood balls. Brood balls under continuous management by dung beetle are rarely contaminated by entomopathogenic fungi compared to abandoned brood balls. On the supposition that dung beetles may benefit from mutualistic bacteria that protect their offspring against fungal pathogens, we evaluated the antifungal activities of bacteria isolated from the dung beetle and brood ball. As a result, bacterial isolates, mainly streptomycetes, manifested potent and broad-spectrum antifungal activity against various fungi, including entomopathogens. Of the isolates, Streptomyces sp. AT67 exhibited pronounced antifungal activities. Culture-dependent and independent approaches show that this strain has occurred continuously in dung beetles that were collected over three years. Moreover, metabolic profiling and chemical investigation demonstrated that the strain produced an antifungal polyene macrocyclic lactam, sceliphrolactam, as a major product. Our findings imply that specific symbiotic bacteria of C. tripartitus are likely to contribute brood ball hygiene by inhibiting fungal parasites in the environment.

Current methods for identifying resource preferences in dung beetles are based on above‐ground trials. Although useful, these methods do not directly investigate resource provisioning of offspring below ground, missing an important part of dung beetle ecology. We tested the potential for UV‐fluorescent and non‐fluorescent coloured glitters to be used as markers for tracing the origin of dung incorporated into brood balls (dung shaped by parental beetles enclosing an egg), and so aid in a more complete understanding of resource use in dung beetles. We tested the effect of glitter addition on brood ball production in two species of tunnelling dung beetles, Onthophagus taurus and Euoniticellus fulvus. There was no effect of glitter addition on brood ball production during no‐choice tests for each species: both species made a similar number of brood balls, regardless of glitter presence or glitter colour. In a separate choice trial, O. taurus showed no preference for dung when presented with four dung pats containing four unique glitter colours. Here we show that glitter can be used as an effective marker of individual brood ball origin in tunnelling dung beetles. This method provides a useful tool for tracking below ground resource use and larval provisioning experiments in dung beetles.

Measuring ecosystem multifunctionality (EMF) could be a valuable method for assessing whether nature‐based solutions, such as introducing non‐native species to benefit ecosystem functioning, yield net positive outcomes. While EMF metrics may provide a coarse overview of the functioning of a system, such metrics can obscure the interactions among multiple simultaneously occurring ecosystem functions. This could limit the predictive value and overall efficacy of EMF metrics for the management of environmental change impacts on ecosystem functioning. We carried out a mesocosm experiment with dung beetle temporal species richness (diversity) treatments in a pasture ecosystem in Aotearoa New Zealand and quantified cascading biotic and abiotic effects of introduced dung beetles (Onthophagus binodis and Onitis alexis) on multiple ecosystem functions. We measured nine individual ecosystem functions affected by dung beetles, including dung removal, total soil carbon, nitrogen, phosphorus, soil microbial respiration, nitrate N, ammonium N, anaerobically mineralisable N and pasture biomass production. We first tested the effects of temporal dung beetle diversity on the nine individual ecosystem functions. We then tested how introduced dung beetle temporal diversity affects ecosystem multifunctionality by calculating EMF metrics using the averaging, threshold and the Hill numbers approaches. Finally, to investigate the underlying interactions among individual functions, we tested the direct and indirect effects of introduced dung beetles on the nine ecosystem functions using structural equation modelling (SEM). Only one out of the nine individual ecosystem functions was significantly affected by dung beetle introductions, whereas five of the six calculated EMF metrics increased significantly with temporal diversity of introduced dung beetles. However, when modelled within an SEM framework, dung beetle temporal diversity was found to directly affect dung removal, but with cascading effects on total N and anaerobically mineralisable N. Our results suggest that introducing and increasing dung beetle temporal diversity enhances the provisioning of multiple ecosystem functions, but that our ability to detect and explain changes in ecosystem multifunctionality is critically dependent on how EMF is quantified. Read the free Plain Language Summary for this article on the Journal blog.

Ball-roller dung beetles of the subfamily Scarabaeinae exhibit two nesting patterns ranging from simple nests (nesting pattern IV) to highly complex nests with parental care (nesting pattern V). Most species of the genus Canthon build a simple nest formed by a single brood ball that is abandoned after oviposition. We studied the nesting behaviour and brood ball architecture of two dung beetle species from South America. Canthon unicolor (Blanchard, 1846) and C. histrio (Le Peletier de Saint-Fargeau & Audinet-and Serville, 1828) construct a shallow nest containing a single brood ball. This brood ball is unique in that it is covered with a thick shield layer made of soil. The shield layer provides to the final brood ball an amorphous external aspect, never described in roller dung beetles. It is less dense than the brood ball layer, and provides, an additional post-ovipositional care. Our results suggest that the nesting behaviour observed in C. unicolor and C. histrio can be considered a new variation of the nesting pattern IV in dung beetles, in which post-ovipositional care through the outer shield layer could increase survival chance of the offspring by protecting them from potential predators, desiccation and a variety of other environmental hazards.

Seeds dispersed by tropical, arboreal mammals are usually deposited singly and without dung or in clumps of fecal material. After dispersal through defecation by mammals, most seeds are secondarily dispersed by dung beetles or consumed by rodents. These post-dispersal, plant-animal interactions are likely to interact themselves, as seeds buried by dung beetles are less likely to be found by rodents than unburied seeds. In a series of three experiments with seeds of 15 species in central Amazonia (Brazil), we determined (1) how presence and amount of dung associated with seeds influences long-term seed fate and seedling establishment, (2) how deeply dung beetles bury seeds and how burial depth affects seedling establishment, and (3) how seed size affects the interaction between seeds, dung beetles, and rodents. Our overall goal was to understand how post-dispersal plant-animal interactions determine the link between primary seed dispersal and seedling establishment. On average, 43% of seeds surrounded by dung were buried by dung beetles, compared to 0% of seeds not surrounded by dung ( n=2,156). Seeds in dung, however, tended to be more prone than bare seeds to predation by rodents. Of seeds in dung, probability of burial was negatively related to seed size and positively related to amount of dung. Burial of seeds decreased the probability of seed predation by rodents three-fold, and increased the probability of seedling establishment two-fold. Mean burial depth was 4 cm (0.5-20 cm) and was not related to seed size, contrary to previous studies. Probability of seedling establishment was negatively correlated with burial depth and not related to seed size at 5 or 10 cm depths. These results illustrate a complex web of interactions among dung beetles, rodents, and dispersed seeds. These interactions affect the probability of seedling establishment and are themselves strongly tied to how seeds are deposited by primary dispersers. More generally, our results emphasize the importance of looking beyond a single type of plant-animal interaction (e.g., seed dispersal or seed predation) to incorporate potential effects of interacting interactions.

Adult dung beetles eat small particles of their food using soft mouthparts, but their larvae have biting jaws with which they chew material in their natal brood ball. It was assumed that microbes supplied by the parents help breakdown food material in the brood ball, which was thought to act as a fermentation chamber. It has been generally accepted that larval dung beetles gain access to nutrients in the dung via symbionts. Various dung treatments used here, including heat sterilisation and anti‐microbials, suggest that the maternal contribution to the brood ball is a pre‐digested meal for the newly hatched larva, and that microbes from the parents are not involved in larval feeding within this group of dung beetles. However, manipulation of the dung by the mother supplied the larva with smaller dung particles from the unsorted dung, and an additional ‘maternal gift’ secretion may provide partially digested dung, both of which affect survival of the larva. This overturns the largely untested dogma that larval dung beetles depend on microbial symbionts from the adults for feeding, but confirms that adult ‘conditioning’ of the dung is important for the larva in selecting out larger dung particles from the brood ball.

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

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 3rd 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.

Loss of large‐bodied mammals across the globe through hunting, habitat degradation, and fragmentation is one of the most significant anthropogenic impacts on the environment. Cascading effects of these extinctions through ecosystems have been little studied, although correlative studies have revealed co‐extinctions in closely linked groups, with implications for ecosystem structure and function. Despite playing important roles in seed dispersal and hence seedling recruitment, mammals have been largely neglected in network studies. Similarly, the role of secondary seed dispersers, such as ants and dung beetles, has been largely unexplored. Most dung beetles rely on mammal feces for feeding and breeding and provide a suite of important ecosystem functions and services. While dung beetle community responses to environmental change have been widely investigated, studies quantifying the network of associations between dung beetle and mammal species are lacking. By developing the first quantitative mammal–dung beetle networks, we address several important knowledge gaps contributing to the understanding of how interactions in networks involving mammals and secondary insect seed dispersers are structured. We use the resulting quantitative interaction networks to model mammal species extinction scenarios to further explore the consequences for dung beetle populations, and the extent to which networks change the strength of interactions through resource switching. Dung beetle feeding and breeding networks did not differ significantly in structure and showed high nestedness and low levels of trophic specialization. Simulations suggested that mammal extinction scenarios based on mammal body mass and mammal dung volume will impact dung beetle populations to a greater extent than random scenarios of mammal loss. Thus, despite their generalist feeding preferences, realistic mammal extinction scenarios have the potential to negatively impact the dung beetle community, which may have consequences for ecosystem functioning.

Organisms are not just passive recipients of environmental pressures but can shape the environment they experience. Yet, the mechanisms and evolutionary implications of such niche construction remain poorly understood. Here, we studied these effects in the gazelle dung beetle (Digitonthophagus gazella). Larvae of this species develop in an underground brood chamber (a 'brood ball') composed of dung, which serves as the sole source of food for a single larva. Throughout its development, the larva extensively modifies its environment by constantly eating, regurgitating and shaping particle sizes within the brood ball. Previous research suggests that these larval manipulations increase environmental quality and nutrient availability. However, how larval modifications affect larval growth and how these modifications differ between species remain poorly understood. We studied the impact of larval environmental modifications by transplanting eggs into previously modified or unmodified environments, whilst controlling for the confounding effect of maternally derived microbes. Additionally, we also studied how D. gazella larvae grow in an environment that was modified by a different species (Onthophagus binodis) to investigate species-specific differences of niche construction. Counter to expectations, we found that larval modifications by conspecifics did not confer a fitness benefit to D. gazella. However, surprisingly, individuals developing in a brood ball modified by a heterospecific individual emerged significantly quicker. These findings provide mixed support that environmental modifications by a larva enhance its growth. Our research adds to the growing literature on the complex interactions between organisms and their environment and how those interactions feed back on organismal development and performance.

Canthon rutilans cyanescens is a telecoprid and coprophagous dung beetle subspecies that builds two types of balls with feeding and nesting purposes. This paperwork describes some behavior and development time characteristics, as well as it analyses the influence of the type and amount of food on this species feeding and reproductive behavior. Adult individuals were sampled in Atlantic Forest areas in southern Brazil (between 2014 and 2016) and they were kept in laboratory conditions within 24 and 27 °C in a 12 hours photoperiod. Development time was observed on brood balls built by 40 couples fed with domestic dog feces. The weight and number of brood and food balls produced by each couple were measured and counted in an experiment with 50 couples fed with feces from distinct mammal’s species as well as in another experiment with 28 couples fed with 1g and 5g of domestic dog feces, distributed into two groups: small and large body size couples. The subspecies’ behavior varied according to the quality of the food resource, with omnivore feces as the best one, possibly due to the higher nutritional quality and microorganism’s diversity. In addition, individuals’ size influenced parental investment and the availability of food resource affected dung beetle’s reproductive success, since, when less food was offered, smaller amounts of food balls and smaller brood balls were built by the adult couples. Our results demonstrated that Canthon rutilans cyanescens has a rapid development and a behavioral plasticity related to the quality and the amount of food.