Polarisation vision in the dark: green-sensitive photoreceptors in the nocturnal ball-rolling dung beetle Escarabaeus satyrus.

Many insects utilise the polarisation pattern of the sky to adjust their travelling directions. The extraction of directional information from this sky-wide cue is mediated by specialised photoreceptors located in the dorsal rim area (DRA). While this part of the eye is known to be sensitive to the ultraviolet, blue or green component of skylight, the latter has only been observed in insects active in dim light. To address the functional significance of green polarisation sensitivity, we define the spectral and morphological adaptations of the DRA in a nocturnal ball-rolling dung beetle-the only family of insects demonstrated to orient to the dim polarisation pattern in the night sky. Intracellular recordings revealed polarisation-sensitive green photoreceptors in the DRA of Escarabaeus satyrus. Behavioural experiments verified the navigational relevance of this finding. To quantify the adaptive value of green sensitivity for celestial orientation at night, we also obtained the polarisation properties of the night sky in the natural habitat of the beetle. Calculations of relative photon catch revealed that under a moonlit sky the green-sensitive DRA photoreceptors can be expected to catch an order of magnitude more photons compared with the UV-sensitive photoreceptors in the main retina. The green-sensitive photoreceptors - which also show a range of morphological adaptations for enhanced sensitivity - provide E. satyrus with a highly sensitive system for the extraction of directional information from the night sky.

Spider dung beetles: coordinated cooperative transport without a predefined destination.

Cooperative transport allows for the transportation of items too large for the capacity of a single individual. Beyond humans, it is regularly employed by ants and social spiders where two or more individuals, with more or less coordinated movements, transport food to a known destination. In contrast to this, pairs of male and female dung beetles successfully transport brood balls to a location unknown to either party at the start of their common journey. We found that, when forced to overcome a series of obstacles in their path, transport efficiency of pairs of beetles was higher than of solo males. To climb tall obstacles with their common ball of dung, the female assisted the leading male in lifting the ball by steadying and pushing it upwards in a 'headstand' position during the climb initiation. Finally, we show that pairs were faster than single beetles in climbing obstacles of different heights. Our results suggest that pairs of Sisyphus beetles cooperate in the transportation of brood balls with coordinated movements, where the male steers and the female primarily assists in lifting the ball. Taken together, this is to our knowledge, the first quantitative study of cooperative food transport without a known goal to aim for.

Erratum: Weighted cue integration for straight-line orientation.

[This corrects the article DOI: 10.1016/j.isci.2022.105207.].

Weighted cue integration for straight-line orientation.

Animals commonly integrate multiple sources of information to guide their behavior. Among insects, previous studies have suggested that the relative reliability of cues affects their weighting in behavior, but have not systematically explored how well alternative integration strategies can account for the observed directional choices. Here, we characterize the directional reliability of an ersatz sun at different elevations and wind at different speeds as guiding cues for a species of ball-rolling dung beetle. The relative reliability is then shown to determine which cue dominates when the cues are put in conflict. We further show through modeling that the results are best explained by continuous integration of the cues as a vector-sum (rather than switching between them) but with non-optimal weighting and small individual biases. The neural circuitry in the insect central complex appears to provide an ideal substrate for this type of vector-sum-based integration mechanism.

The interplay of directional information provided by unpolarised and polarised light in the heading direction network of the diurnal dung beetle Kheper lamarcki.

The sun is the most prominent source of directional information in the heading direction network of the diurnal, ball-rolling dung beetle Kheper lamarcki. If this celestial body is occluded from the beetle's field of view, the distribution of the relative weight between the directional cues that remain shifts in favour of the celestial pattern of polarised light. In this study, we continue to explore the interplay of the sun and polarisation pattern as directional cues in the heading direction network of K. lamarcki. By systematically altering the intensity and degree of the two cues, we effectively change the relative reliability as they appear to the dung beetle. The response of the beetle to these modifications allows us to closely examine how the weighting relationship of these two sources of directional information is influenced and altered in the heading direction network of the beetle. We conclude that the process by which K. lamarcki relies on directional information is very likely done based on Bayesian reasoning, where directional information conveying the highest certainty at a particular moment is afforded the greatest weight.

The finely defined shift work schedule of dung beetles and their eye morphology.

In nature, nothing is wasted, not even waste. Dung, composed of metabolic trash and leftovers of food, is a high-quality resource and the object of fierce competition. Over 800 dung beetle species (Scarabaeinae) compete in the South African dung habitat and more than 100 species can colonize a single dung pat. To coexist in the same space, using the same food, beetles divide the day between them. However, detailed diel activity periods and associated morphological adaptations have been largely overlooked in these dung-loving insects. To address this, we used a high-frequency trapping design to establish the diel activity period of 44 dung beetle species in their South Africa communities. This allowed us to conclude that the dung beetles show a highly refined temporal partitioning strategy, with differences in peak of activity even within the diurnal, crepuscular, and nocturnal guilds, independent of nesting behavior and taxonomic classification. We further analyzed differences in eye and body size of our 44 model species and describe their variability in external eye morphology. In general, nocturnal species are bigger than crepuscular and diurnal species, and as expected, the absolute and relative eye size is greatest in nocturnal species, followed by crepuscular and then diurnal species. A more surprising finding was that corneal structure (smooth or facetted) is influenced by the activity period of the species, appearing flat in the nocturnal species and highly curved in the diurnal species. The role of the canthus-a cuticular structure that partially or completely divides the dung beetle eye into dorsal and ventral parts-remains a mystery, but the large number of species investigated in this study nevertheless allowed us to reject any correlation between its presence and the nesting behavior or time of activity of the beetles.

Compass Cue Integration and Its Relation to the Visual Ecology of Three Tribes of Ball-Rolling Dung Beetles.

To guide their characteristic straight-line orientation away from the dung pile, ball-rolling dung beetles steer according to directional information provided by celestial cues, which, among the most relevant are the sun and polarised skylight. Most studies regarding the use of celestial cues and their influence on the orientation system of the diurnal ball-rolling beetle have been performed on beetles of the tribe Scarabaeini living in open habitats. These beetles steer primarily according to the directional information provided by the sun. In contrast, Sisyphus fasciculatus, a species from a different dung-beetle tribe (the Sisyphini) that lives in habitats with closely spaced trees and tall grass, relies predominantly on directional information from the celestial pattern of polarised light. To investigate the influence of visual ecology on the relative weight of these cues, we studied the orientation strategy of three different tribes of dung beetles (Scarabaeini, Sisyphini and Gymnopleurini) living within the same biome, but in different habitat types. We found that species within a tribe share the same orientation strategy, but that this strategy differs across the tribes; Scarabaeini, living in open habitats, attribute the greatest relative weight to the directional information from the sun; Sisyphini, living in closed habitats, mainly relies on directional information from polarised skylight; and Gymnopleurini, also living in open habitats, appear to weight both cues equally. We conclude that, despite exhibiting different body size, eye size and morphology, dung beetles nevertheless manage to solve the challenge of straight-line orientation by weighting visual cues that are particular to the habitat in which they are found. This system is however dynamic, allowing them to operate equally well even in the absence of the cue given the greatest relative weight by the particular species.

Light pollution forces a change in dung beetle orientation behavior.

Increasing global light pollution1,2 threatens the night-time darkness to which most animals are adapted. Light pollution can have detrimental effects on behavior,3-5 including by disrupting the journeys of migratory birds,5,6 sand hoppers,7-9 and moths.10 This is particularly concerning, since many night-active species rely on compass information in the sky, including the moon,11,12 the skylight polarization pattern,13,14 and the stars,15 to hold their course. Even animals not directly exposed to streetlights and illuminated buildings may still experience indirect light pollution in the form of skyglow,3,4 which can extend far beyond urban areas.1,2 While some recent research used simulated light pollution to estimate how skyglow may affect orientation behavior,7-9 the consequences of authentic light pollution for celestial orientation have so far been neglected. Here, we present the results of behavioral experiments at light-polluted and dark-sky sites paired with photographic measurements of each environment. We find that light pollution obscures natural celestial cues and induces dramatic changes in dung beetle orientation behavior, forcing them to rely on bright earthbound beacons in place of their celestial compass. This change in behavior results in attraction toward artificial lights, thereby increasing inter-individual competition and reducing dispersal efficiency. For the many other species of insect, bird, and mammal that rely on the night sky for orientation and migration, these effects could dramatically hinder their vital night-time journeys.

Elevated atmospheric CO2 adversely affects a dung beetle's development: Another potential driver of decline in insect numbers?

Insect declines have been attributed to several drivers such as habitat loss, climate change, invasive alien species and insecticides. However, in the global context, these effects remain patchy, whereas insect losses appear to be consistent worldwide. Increases in atmospheric CO2 concentrations are known to have indirect effects on herbivorous insects, but the effects on other insects are largely unexplored. We wondered if elevated atmospheric CO2 (eCO2 ) could influence the growth and survival of insects, not via rising temperature, nor through their changes in food quality, but by other means. Rearing tunnelling dung beetle Euoniticellus intermedius (Reiche, 1848) at pre-industrial (250 parts per million [ppm]), current (400 ppm) and eCO2 levels (600 and 800 ppm), we found that exposure to eCO2 resulted in longer developmental times and increased mortality. Elevated CO2 also caused reduction of adult size and mass which is detrimental to dung beetle fitness. Additional results showed associated increases in CO2 levels inside dung brood balls, dung pH and respiration rates of the soil surrounding the developing dung beetles (CO2 flux). We thus hypothesize that elevated CO2 increases competition for O2 and nutrients between soil microbiota and subterranean insects. Given that many insect orders spend at least part of their life underground, our findings indicate the possibility of a negative ubiquitous effect of eCO2 on a large portion of the earth's insect biota. These findings therefore suggest an important area for future research on the soil community in the context of atmospheric change.

Straight-line orientation in the woodland-living beetle Sisyphus fasciculatus.

To transport their balls of dung along a constant bearing, diurnal savannah-living dung beetles rely primarily on the sun for compass information. However, in more cluttered environments, such as woodlands, this solitary compass cue is frequently hidden from view by surrounding vegetation. In these types of habitats, insects can, instead, rely on surrounding landmarks, the canopy pattern, or wide-field celestial cues, such as polarised skylight, for directional information. Here, we investigate the compass orientation strategy behind straight-line orientation in the diurnal woodland-living beetle Sisyphus fasciculatus. We found that, when manipulating the direction of polarised skylight, Si. fasciculatus responded to this change with a similar change in bearing. However, when the apparent position of the sun was moved, the woodland-living beetle did not change its direction of travel. In contrast, the savannah-living beetle Scarabaeus lamarcki responded to the manipulation of the solar position with a corresponding change in bearing. These results suggest that the dominant compass cue used for straight-line orientation in dung beetles may be determined by the celestial cue that is most prominent in their preferred habitat.

The effect of step size on straight-line orientation.

Moving along a straight path is a surprisingly difficult task. This is because, with each ensuing step, noise is generated in the motor and sensory systems, causing the animal to deviate from its intended route. When relying solely on internal sensory information to correct for this noise, the directional error generated with each stride accumulates, ultimately leading to a curved path. In contrast, external compass cues effectively allow the animal to correct for errors in its bearing. Here, we studied straight-line orientation in two different sized dung beetles. This allowed us to characterize and model the size of the directional error generated with each step, in the absence of external visual compass cues (motor error) as well as in the presence of these cues (compass and motor errors). In addition, we model how dung beetles balance the influence of internal and external orientation cues as they orient along straight paths under the open sky. We conclude that the directional error that unavoidably accumulates as the beetle travels is inversely proportional to the step size of the insect, and that both beetle species weigh the two sources of directional information in a similar fashion.

Eye and wing structure closely reflects the visual ecology of dung beetles.

An important resource partitioning strategy allowing dung beetles to coexist in the same habitat, while utilising the same food, is species' separation of activity times. After establishing the diel activity period of three closely related, co-occurring dung beetles, we examined their eye and wing morphology. Absolute and relative eye size, and facet size were greater in the nocturnal Escarabaeus satyrus, followed by the crepuscular Scarabaeus zambesianus and then the diurnal Kheper lamarcki. The diurnal K. lamarcki had the highest wing aspect ratio (long, narrow wings), followed by the crepuscular S. zambesianus and the nocturnal E. satyrus (short, broad wings), suggesting that dim-light active species fly slower than diurnal species. In addition, the two species active in dim light had a lower wing loading than the diurnal species, indicating the need for greater manoeuvrability in the dark. Analyses of wing shape revealed that the diurnal K. lamarcki wing had a proportionally larger jugal and anal region than both dim light species. Our results show that different species of dung beetles have a combination of optical and morphological wing adaptations to support their foraging activities in diverse light conditions.

Dung beetle (Coleoptera: Scarabaeoidea) assemblages in the western Italian Alps: benchmark data for land use monitoring.

BACKGROUND: Traditional agro-pastoral practices are in decline over much of the Alps (MacDonald et al. 2000), leading to shrub and tree encroachment, and this represents one of the main threats for the conservation of alpine biodiversity, as many plant and animal species are dependent on the presence of semi-natural open habitats. However, quantifying this environmental change and assessing its impact on biodiversity may be difficult, especially in the context of sparse historical survey data. The accessibility of contemporary data about local biodiversity surveys in general, and indicator taxa in particular, is an essential consideration for planning future evaluations of conservation status in the Alps and for conservation plans that use ecological indicators to monitor temporal changes in biodiversity. Dung beetles are important ecosystem service providers (Nichols et al. 2008) that have been assessed as a good ecological indicator taxon in several studies (reviewed by Nichols and Gardner 2011), and although the Alps is perhaps one of the best-studied regions in respect of dung beetles, there are still only eight readily-accessible publications. We have augmented and comprehensively reviewed the data from these publications. NEW INFORMATION: We first provide data about changes on a temporal scale of seasons in a dung beetle community in the western Italian Alps, an issue that has to be addressed in the local assemblages because it would affect regional biomonitoring and conservation research. This survey of 12 099 individuals belonging to 22 species illustrates a distinct seasonal pattern at a single site. Second, we collate the results of 13 published surveys of the presence of 46 species of dung beetles in 11 valleys in the western Italian Alps in the period from 2005 to 2012, a period of accelerated change in land use that started around 1945 (MacDonald et al. 2000). Because ten of the surveys used baited pitfall traps and four more used manual collection of specimens, the abundance data were not strictly comparable and they were therefore transformed to binary data (presence-or-absence records) with measures of sampling effort. The results illustrate both spatial variation and temporal variation at the scale of years.Because of the importance of dung beetles in agro-pastoral ecosystems and the high sensitivity of montane ecosystems to climate change, these spatially and temporally explicit data sets provide important baseline information about western Italian Alpine dung beetles for investigations of the effects of land use change under ongoing climate change scenarios.

The effects of body mass on dung removal efficiency in dung beetles.

Understanding of the role of body mass in structural-functional relationships is pressing, particularly because species losses often occur non-randomly with respect to body size. Our study examined the effects of dung beetle body mass on dung removal at two levels. First, we used the lab experiment to evaluate the efficiency of eight dung beetle species belonging to two functional groups (tunnelers, dwellers) on dung removal. Second, the same species employed in the lab were used in field mesocosms to examine the effects of the two functional groups on dung removal maintaining realistic differences in the total body mass between tunneler and dweller assemblages. Furthermore, the experimental assemblages contained one and four species within each functional group, so the effect of body mass heterogeneity was examined. We used a statistical approach (offset method) which took into account a priori constraints due to the study design allowing us to analyse the effect of larger species in mesocosm style experiments. Body size played a crucial role in dung removal: large beetles were more efficient than small ones and the percentage of removed dung increased with higher body mass heterogeneity. Tunnelers were more efficient than dwellers over both short and long time periods (one month and one year). Significant effects of dwellers were found only after one year. Moreover, our study showed that not including the body mass as an offset in the model resulted in sometimes different results, as the offset expresses dung removal independently of the body mass. This approach confirmed that body size is likely a pivotal factor controlling dung removal efficiency at multiple levels, from single species to overall dung beetle assemblages. Even though other specific traits should be examined, this study has begun to address the consequences of losing individuals with specific traits that are especially sensitive to perturbations.

Pastoral practices to reverse shrub encroachment of sub-alpine grasslands: dung beetles (coleoptera, scarabaeoidea) respond more quickly than vegetation.

In recent decades, pastoral abandonment has produced profound ecological changes in the Alps. In particular, the reduction in grazing has led to extensive shrub encroachment of semi-natural grasslands, which may represent a threat to open habitat biodiversity. To reverse shrub encroachment, we assessed short-term effects of two different pastoral practices on vegetation and dung beetles (Coleoptera, Scarabaeoidea). Strategic placement of mineral mix supplements (MMS) and arrangement of temporary night camp areas (TNCA) for cattle were carried out during summer 2011 in the Val Troncea Natural Park, north-western Italian Alps. In 2012, one year after treatment, a reduction in shrub cover and an increase in bare ground cover around MMS sites was detected. A more intense effect was detected within TNCA through increases in forage pastoral value, and in the cover and height of the herbaceous layer. Immediately after treatment, changes in dung beetle diversity (total abundance, species richness, Shannon diversity, taxonomic and functional diversity) showed a limited disturbance effect caused by high cattle density. In contrast, dung beetle diversity significantly increased one year later both at MMS and TNCA sites, with a stronger effect within TNCA. Multivariate Regression Trees and associated Indicator Value analyses showed that some ecologically relevant dung beetle species preferred areas deprived of shrub vegetation. Our main conclusions are: i) TNCA are more effective than MMS in terms of changes to vegetation and dung beetles, ii) dung beetles respond more quickly than vegetation to pastoral practices, and iii) the main driver of the rapid response by dung beetles is the removal of shrubs. The resulting increase in dung beetle abundance and diversity, which are largely responsible for grassland ecosystem functioning, may have a positive effect on meso-eutrophic grassland restoration. Shrub encroachment in the Alps may therefore be reversed, and restoration of grassland enhanced, by using appropriate pastoral practices.