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.

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.

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.

Orienting to polarized light at night - matching lunar skylight to performance in a nocturnal beetle.

For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal's natural environment must be above the threshold for detection and interpretation. Here, we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific reference to the range of degrees of polarization measured in the night sky. An effect of lunar phase on the degree of polarization of skylight was found, with smaller illuminated fractions of the moon's surface corresponding to lower degrees of polarization in the night sky. We found that the South African dung beetle Escarabaeus satyrus can orient to polarized light for a range of degrees of polarization similar to that observed in diurnal insects, reaching a lower threshold between 0.04 and 0.32, possibly as low as 0.11. For degrees of polarization lower than 0.23, as measured on a crescent moon night, orientation performance was considerably weaker than that observed for completely linearly polarized stimuli, but was nonetheless stronger than in the absence of polarized light.

Neural coding underlying the cue preference for celestial orientation.

Diurnal and nocturnal African dung beetles use celestial cues, such as the sun, the moon, and the polarization pattern, to roll dung balls along straight paths across the savanna. Although nocturnal beetles move in the same manner through the same environment as their diurnal relatives, they do so when light conditions are at least 1 million-fold dimmer. Here, we show, for the first time to our knowledge, that the celestial cue preference differs between nocturnal and diurnal beetles in a manner that reflects their contrasting visual ecologies. We also demonstrate how these cue preferences are reflected in the activity of compass neurons in the brain. At night, polarized skylight is the dominant orientation cue for nocturnal beetles. However, if we coerce them to roll during the day, they instead use a celestial body (the sun) as their primary orientation cue. Diurnal beetles, however, persist in using a celestial body for their compass, day or night. Compass neurons in the central complex of diurnal beetles are tuned only to the sun, whereas the same neurons in the nocturnal species switch exclusively to polarized light at lunar light intensities. Thus, these neurons encode the preferences for particular celestial cues and alter their weighting according to ambient light conditions. This flexible encoding of celestial cue preferences relative to the prevailing visual scenery provides a simple, yet effective, mechanism for enabling visual orientation at any light intensity.

Camera-based automated monitoring of flying insects in the wild (Camfi). II. flight behaviour and long-term population monitoring of migratory Bogong moths in Alpine Australia.

Introduction: The Bogong moth Agrotis infusa is well known for its remarkable annual round-trip migration from its breeding grounds across eastern and southern Australia to its aestivation sites in the Australian Alps, to which it provides an important annual influx of nutrients. Over recent years, we have benefited from a growing understanding of the navigational abilities of the Bogong moth. Meanwhile, the population of Bogong moths has been shrinking. Recently, the ecologically and culturally important Bogong moth was listed as endangered by the IUCN Red List, and the establishment of a program for long-term monitoring of its population has been identified as critical for its conservation. Methods: Here, we present the results of two years of monitoring of the Bogong moth population in the Australian Alps using recently developed methods for automated wildlife-camera monitoring of flying insects, named Camfi. While in the Alps, some moths emerge from the caves in the evening to undertake seemingly random flights, filling the air with densities in the dozens per cubic metre. The purpose of these flights is unknown, but they may serve an important role in Bogong moth navigation. Results: We found that these evening flights occur throughout summer and are modulated by daily weather factors. We present a simple heuristic model of the arrival to and departure from aestivation sites by Bogong moths, and confirm results obtained from fox-scat surveys which found that aestivating Bogong moths occupy higher elevations as the summer progresses. Moreover, by placing cameras along two elevational transects below the summit of Mt. Kosciuszko, we found that evening flights were not random, but were systematically oriented in directions relative to the azimuth of the summit of the mountain. Finally, we present the first recorded observations of the impact of bushfire smoke on aestivating Bogong moths - a dramatic reduction in the size of a cluster of aestivating Bogong moths during the fire, and evidence of a large departure from the fire-affected area the day after the fire. Discussion: Our results highlight the challenges of monitoring Bogong moths in the wild and support the continued use of automated camera-based methods for that purpose.

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.

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.

Stellar performance: mechanisms underlying Milky Way orientation in dung beetles.

Nocturnal dung beetles (Scarabaeus satyrus) are currently the only animals that have been demonstrated to use the Milky Way for reliable orientation. In this study, we tested the capacity of S. satyrus to orient under a range of artificial celestial cues, and compared the properties of these cues with images of the Milky Way simulated for a beetle's visual system. We find that the mechanism that permits accurate stellar orientation under the Milky Way is based on an intensity comparison between different regions of the Milky Way. We determined the beetles' contrast sensitivity for this task in behavioural experiments in the laboratory, and found that the resulting threshold of 13% is sufficient to detect the contrast between the southern and northern arms of the Milky Way under natural conditions. This mechanism should be effective under extremely dim conditions and on nights when the Milky Way forms a near symmetrical band that crosses the zenith. These findings are discussed in the context of studies of stellar orientation in migratory birds and itinerant seals.This article is part of the themed issue 'Vision in dim light'.

A Snapshot-Based Mechanism for Celestial Orientation.

In order to protect their food from competitors, ball-rolling dung beetles detach a piece of dung from a pile, shape it into a ball, and roll it away along a straight path [1]. They appear to rely exclusively on celestial compass cues to maintain their bearing [2-8], but the mechanism that enables them to use these cues for orientation remains unknown. Here, we describe the orientation strategy that allows dung beetles to use celestial cues in a dynamic fashion. We tested the underlying orientation mechanism by presenting beetles with a combination of simulated celestial cues (sun, polarized light, and spectral cues). We show that these animals do not rely on an innate prediction of the natural geographical relationship between celestial cues, as other navigating insects seem to [9, 10]. Instead, they appear to form an internal representation of the prevailing celestial scene, a "celestial snapshot," even if that scene represents a physical impossibility for the real sky. We also find that the beetles are able to maintain their bearing with respect to the presented cues only if the cues are visible when the snapshot is taken. This happens during the "dance," a behavior in which the beetle climbs on top of its ball and rotates about its vertical axis [11]. This strategy for reading celestial signals is a simple but efficient mechanism for straight-line orientation.