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.

An Intra-Tissue Radiometry Microprobe for Measuring Radiance In Situ in Living Tissue.

Organisms appear opaque largely because their outer tissue layers are strongly scattering to incident light; strongly absorbing pigments, such as blood, typically have narrow absorbances, such that the mean free path of light outside the absorbance peaks can be quite long. As people cannot see through tissue, they generally imagine that tissues like the brain, fat, and bone contain little or no light. However, photoresponsive opsin proteins are expressed within many of these tissues, and their functions are poorly understood. Radiance internal to tissue is also important for understanding photosynthesis. For example, giant clams are strongly absorbing yet maintain a dense population of algae deep in the tissue. Light propagation through systems like sediments and biofilms can be complex, and these communities can be major contributors to ecosystem productivity. Therefore, a method for constructing optical micro-probes for measuring scalar irradiance (photon flux intersecting a point) and downwelling irradiance (photon flux crossing a plane perpendicularly) to better understand these phenomena inside living tissue has been developed. This technique is also tractable in field laboratories. These micro-probes are made from heat-pulled optical fibers that are then secured in pulled glass pipettes. To change the angular acceptance of the probe, a 10-100 µm sized sphere of UV-curable epoxy mixed with titanium dioxide is then secured to the end of a pulled, trimmed fiber. The probe is inserted into living tissue, and its position is controlled using a micromanipulator. These probes are capable of measuring in situ tissue radiance at spatial resolutions of 10-100 µm or on the scale of single cells. These probes were used to characterize the light reaching the adipose and brain cells 4 mm below the skin of a living mouse and to characterize the light reaching similar depths within living algae-rich giant clam tissue.

The balbyter ant Camponotus fulvopilosus combines several navigational strategies to support homing when foraging in the close vicinity of its nest.

Many insects rely on path integration to define direct routes back to their nests. When shuttling hundreds of meters back and forth between a profitable foraging site and a nest, navigational errors accumulate unavoidably in this compass- and odometer-based system. In familiar terrain, terrestrial landmarks can be used to compensate for these errors and safely guide the insect back to its nest with pin-point precision. In this study, we investigated the homing strategies employed by Camponotus fulvopilosus ants when repeatedly foraging no more than 1.25 m away from their nest. Our results reveal that the return journeys of the ants, even when setting out from a feeder from which the ants could easily get home using landmark information alone, are initially guided by path integration. After a short run in the direction given by the home vector, the ants then switched strategies and started to steer according to the landmarks surrounding their nest. We conclude that even when foraging in the close vicinity of its nest, an ant still benefits from its path-integrated vector to direct the start of its return journey.

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.

Cold-induced anesthesia impairs path integration memory in dung beetles.

Path integration is a general mechanism used by many animals to maintain an updated record of their position in relation to a set reference point.1-11 To do this, they continually integrate direction and distance information into a memorized home vector. What remains unclear is how this vector is stored, maintained, and utilized for successful navigation. A recent computational model based on the neuronal circuitry of the insect central complex suggests that home vector memories are encoded across a set of putative memory neurons and maintained through ongoing recurrent neural activity.12 To better understand the nature of the home vector memory and experimentally assess underlying mechanisms for maintaining it, we performed a series of experiments on the path integrating dung beetle Scarabaeus galenus.13 We found that, while the directional component of the home vector was maintained for up to 1 h, the distance component of the vector memory decreased gradually over time. Using cold-induced anesthesia, we disrupted the neural activity of beetles that had stored a home vector of known length and direction. This treatment diminished both components of the home vector memory, but by different amounts-the homing beetles lost their distance memory before their directional memory. Together, these findings present new insights into the functional properties of home vector memories and provide the first empirical evidence that a biological process that can be disrupted by cold-induced anesthesia is essential to support homing by path integration.

A dung beetle that path integrates without the use of landmarks.

Unusual amongst dung beetles, Scarabaeus galenus digs a burrow that it provisions by making repeated trips to a nearby dung pile. Even more remarkable is that these beetles return home moving backwards, with a pellet of dung between their hind legs. Here, we explore the strategy that S. galenus uses to find its way home. We find that, like many other insects, they use path integration to calculate the direction and distance to their home. If they fail to locate their burrow, the beetles initiate a distinct looping search behaviour that starts with a characteristic sharp turn, we have called a 'turning point'. When homing beetles are passively displaced or transferred to an unfamiliar environment, they initiate a search at a point very close to the location of their fictive burrow-that is, a spot at the same relative distance and direction from the pick-up point as the original burrow. Unlike other insects, S. galenus do not appear to supplement estimates of the burrow location with landmark information. Thus, S. galenus represents a rare case of a consistently backward-homing animal that does not use landmarks to augment its path integration strategy.

The mirror-based eyes of scallops demonstrate a light-evoked pupillary response.

Light levels in terrestrial and shallow-water environments can vary by ten orders of magnitude between clear days and overcast nights. Light-evoked pupillary responses help the eyes of animals perform optimally under these variable light conditions by balancing trade-offs between sensitivity and resolution [1]. Here, we document that the mirror-based eyes of the bay scallop Argopecten irradians and the sea scallop Placopecten magellanicus have pupils that constrict to ∼60% of their fully dilated areas within several minutes of light exposure. The eyes of scallops contain two separate retinas and our ray-tracing model indicates that, compared to eyes with fully constricted pupils, eyes from A. irradians with fully dilated pupils provide approximately three times the sensitivity and half the spatial resolution at the distal retina and five times the sensitivity and one third the spatial resolution at the proximal retina. We also identify radial and circular actin fibers associated with the corneas of A. irradians that may represent muscles whose contractions dilate and constrict the pupil, respectively.

Losing focus: how lens position and viewing angle affect the function of multifocal lenses in fishes.

Light rays of different wavelengths are focused at different distances when they pass through a lens (longitudinal chromatic aberration [LCA]). For animals with color vision this can pose a serious problem, because in order to perceive a sharp image the rays must be focused at the shallow plane of the photoreceptor's outer segments in the retina. A variety of fish and tetrapods have been found to possess multifocal lenses, which correct for LCA by assigning concentric zones to correctly focus specific wavelengths. Each zone receives light from a specific beam entrance position (BEP) (the lateral distance between incoming light and the center of the lens). Any occlusion of incoming light at specific BEPs changes the composition of the wavelengths that are correctly focused on the retina. Here, we calculated the effect of lens position relative to the plane of the iris and light entering the eye at oblique angles on how much of the lens was involved in focusing the image on the retina (measured as the availability of BEPs). We used rotational photography of fish eyes and mathematical modeling to quantify the degree of lens occlusion. We found that, at most lens positions and viewing angles, there was a decrease of BEP availability and in some cases complete absence of some BEPs. Given the implications of these effects on image quality, we postulate that three morphological features (aphakic spaces, curvature of the iris, and intraretinal variability in spectral sensitivity) may, in part, be adaptations to mitigate the loss of spectral image quality in the periphery of the eyes of fishes.

Comment on "Open-ocean fish reveal an omnidirectional solution to camouflage in polarized environments".

Brady et al (Reports, 20 November 2015, p. 965) claimed that the silvery sides of certain fish are cryptic when viewed by animals with polarization sensitivity, which they termed "polarocrypsis." After examining their evidence, we find this claim to be unsupported due to (i) pseudoreplication, (ii) confounding polarization contrast with intensity contrast, and (iii) measurements taken at very shallow depths.

Examining the Effects of Chromatic Aberration, Object Distance, and Eye Shape on Image-Formation in the Mirror-Based Eyes of the Bay Scallop Argopecten irradians.

The eyes of scallops form images using a concave spherical mirror and contain two separate retinas, one layered on top of the other. Behavioral and electrophysiological studies indicate that the images formed by these eyes have angular resolutions of about 2°. Based on previous ray-tracing models, it has been thought that the more distal of the two retinas lies near the focal point of the mirror and that the proximal retina, positioned closer to the mirror at the back of the eye, receives light that is out-of-focus. Here, we propose three mechanisms through which both retinas may receive focused light: (1) chromatic aberration produced by the lens may cause the focal points for longer and shorter wavelengths to fall near the distal and proximal retinas, respectively; (2) focused light from near and far objects may fall on the distal and proximal retinas, respectively; and (3) the eyes of scallops may be dynamic structures that change shape to determine which retina receives focused light. To test our hypotheses, we used optical coherence tomography (OCT), a method of near-infrared optical depth-ranging, to acquire virtual cross-sections of live, intact eyes from the bay scallop Argopecten irradians Next, we used a custom-built ray-tracing model to estimate the qualities of the images that fall on an eye's distal and proximal retinas as functions of the wavelengths of light entering the eye (400-700 nm), object distances (0.01-1 m), and the overall shape of the eye. When we assume 550 nm wavelength light and object distances greater than 0.01 m, our model predicts that the angular resolutions of the distal and proximal retinas are 2° and 7°, respectively. Our model also predicts that neither chromatic aberration nor differences in object distance lead to focused light falling on the distal and proximal retinas simultaneously. However, if scallops can manipulate the shapes of their eyes, perhaps through muscle contractions, we speculate that they may be able to influence the qualities of the images that fall on their proximal retinas and-to a lesser extent-those that fall on their distal retinas as well.

Polarization vision seldom increases the sighting distance of silvery fish.

Although the function of polarization vision, the ability to discern the polarization characteristics of light, is well established in many terrestrial and benthic species, its purpose in pelagic species (squid and certain fish and crustaceans) is poorly understood [1]. A long-held hypothesis is that polarization vision in open water is used to break the mirror camouflage of silvery fish, as biological mirrors can change the polarization of reflected light [2,3]. Although, the addition of polarization information may increase the conspicuousness of silvery fish at close range, direct evidence that silvery fish - or indeed any pelagic animal - are visible at longer distances using polarization vision rather than using radiance (i.e. brightness) vision is lacking. Here we show, using in situ polarization imagery and a new visual detection model, that polarization vision does not in fact appear to allow viewers to see silvery fish at greater distances.

Intuitive representation of photopolarimetric data using the polarization ellipse.

Photopolarimetry is the spatial characterization of light polarization. Unlike intensity or wavelength, we are largely insensitive to polarization and therefore find it hard to explore the multidimensional data that photopolarimetry produces (two spatial dimensions plus four polarization dimensions). Many different ways for presenting and exploring this modality of light have been suggested. Most of these ignore circular polarization, include multiple image panes that make correlating structure with polarization difficult, and obscure the main trends with overly detailed information and often misleading colour maps. Here, we suggest a novel way for presenting the main results from photopolarimetric analyses. By superimposing a grid of polarization ellipses onto the RGB image, the full polarization state of each cell is intuitively conveyed to the reader. This method presents linear and circular polarization as well as ellipticity in a graphical manner, does not require multiple panes, facilitates the correlation between structure and polarization, and requires the addition of only three novel colours. We demonstrate its usefulness in a biological context where we believe it would be most relevant.

Circularly Polarized Light as a Communication Signal in Mantis Shrimps.

Animals that communicate using conspicuous body patterns face a trade-off between desired detection by intended receivers and undesired detection from eavesdropping predators, prey, rivals, or parasites. In some cases, this trade-off favors the evolution of signals that are both hidden from predators and visible to conspecifics. Animals may produce covert signals using a property of light that is invisible to those that they wish to evade, allowing them to hide in plain sight (e.g., dragonfish can see their own, otherwise rare, red bioluminescence). The use of the polarization of light is a good example of a potentially covert communication channel, as very few vertebrates are known to use polarization for object-based vision. However, even these patterns are vulnerable to eavesdroppers, as sensitivity to the linearly polarized component of light is widespread among invertebrates due to their intrinsically polarization sensitive photoreceptors. Stomatopod crustaceans appear to have gone one step further in this arms race and have evolved a sensitivity to the circular polarization of light, along with body patterns producing it. However, to date we have no direct evidence that any of these marine crustaceans use this modality to communicate with conspecifics. We therefore investigated circular polarization vision of the mantis shrimp Gonodactylaceus falcatus and demonstrate that (1) the species produces strongly circularly polarized body patterns, (2) they discriminate the circular polarization of light, and (3) that they use circular polarization information to avoid occupied burrows when seeking a refuge.

Cuttlefish Sepia officinalis Preferentially Respond to Bottom Rather than Side Stimuli When Not Allowed Adjacent to Tank Walls.

Cuttlefish are cephalopods capable of rapid camouflage responses to visual stimuli. However, it is not always clear to what these animals are responding. Previous studies have found cuttlefish to be more responsive to lateral stimuli rather than substrate. However, in previous works, the cuttlefish were allowed to settle next to the lateral stimuli. In this study, we examine whether juvenile cuttlefish (Sepia officinalis) respond more strongly to visual stimuli seen on the sides versus the bottom of an experimental aquarium, specifically when the animals are not allowed to be adjacent to the tank walls. We used the Sub Sea Holodeck, a novel aquarium that employs plasma display screens to create a variety of artificial visual environments without disturbing the animals. Once the cuttlefish were acclimated, we compared the variability of camouflage patterns that were elicited from displaying various stimuli on the bottom versus the sides of the Holodeck. To characterize the camouflage patterns, we classified them in terms of uniform, disruptive, and mottled patterning. The elicited camouflage patterns from different bottom stimuli were more variable than those elicited by different side stimuli, suggesting that S. officinalis responds more strongly to the patterns displayed on the bottom than the sides of the tank. We argue that the cuttlefish pay more attention to the bottom of the Holodeck because it is closer and thus more relevant for camouflage.

Photosymbiotic giant clams are transformers of solar flux.

'Giant' tridacnid clams have evolved a three-dimensional, spatially efficient, photodamage-preventing system for photosymbiosis. We discovered that the mantle tissue of giant clams, which harbours symbiotic nutrition-providing microalgae, contains a layer of iridescent cells called iridocytes that serve to distribute photosynthetically productive wavelengths by lateral and forward-scattering of light into the tissue while back-reflecting non-productive wavelengths with a Bragg mirror. The wavelength- and angle-dependent scattering from the iridocytes is geometrically coupled to the vertically pillared microalgae, resulting in an even re-distribution of the incoming light along the sides of the pillars, thus enabling photosynthesis deep in the tissue. There is a physical analogy between the evolved function of the clam system and an electric transformer, which changes energy flux per area in a system while conserving total energy. At incident light levels found on shallow coral reefs, this arrangement may allow algae within the clam system to both efficiently use all incident solar energy and avoid the photodamage and efficiency losses due to non-photochemical quenching that occur in the reef-building coral photosymbiosis. Both intra-tissue radiometry and multiscale optical modelling support our interpretation of the system's photophysics. This highly evolved 'three-dimensional' biophotonic system suggests a strategy for more efficient, damage-resistant photovoltaic materials and more spatially efficient solar production of algal biofuels, foods and chemicals.

Simplifying numerical ray tracing for characterization of optical systems.

Ray tracing, a computational method for tracing the trajectories of rays of light through matter, is often used to characterize mechanical or biological visual systems with aberrations that are larger than the effect of diffraction inherent in the system. For example, ray tracing may be used to calculate geometric point spread functions (PSFs), which describe the image of a point source after it passes through an optical system. Calculating a geometric PSF is useful because it gives an estimate of the detail and quality of the image formed by a given optical system. However, when using ray tracing to calculate a PSF, the accuracy of the estimated PSF directly depends on the number of discrete rays used in the calculation; higher accuracies may require more computational power. Furthermore, adding optical components to a modeled system will increase its complexity and require critical modifications so that the model will describe the system correctly, sometimes necessitating a completely new model. Here, we address these challenges by developing a method that represents rays of light as a continuous function that depends on the light's initial direction. By utilizing Chebyshev approximations (via the chebfun toolbox in MATLAB) for the implementation of this method, we greatly simplified the calculations for the location and direction of the rays. This method provides high precision and fast calculation speeds that allow the characterization of any symmetrical optical system (with a centered point source) in an analytical-like manner. Next, we demonstrate our methods by showing how they can easily calculate PSFs for complicated optical systems that contain multiple refractive and/or reflective interfaces.

Visual acuity in pelagic fishes and mollusks.

In the sea, visual scenes change dramatically with depth. At shallow and moderate depths (<1,000 m), there is enough light for animals to see the surfaces and shapes of prey, predators, and conspecifics. This changes below 1,000 m, where no downwelling daylight remains and the only source of light is bioluminescence. These different visual scenes require different visual adaptations and eye morphologies. In this study we investigate how the optical characteristics of animal lenses correlate with depth and ecology. We measured the radius, focal length, and optical quality of the lenses of pelagic fishes, cephalopods, and a gastropod using a custom-built apparatus. The hatchetfishes (Argyropelecus aculeatus and Sternoptyx diaphana) and the barrel-eye (Opisthoproctus soleatus) were found to have the best lenses, which may allow them to break the counterillumination camouflage of their prey. The heteropod lens had unidirectional aberrations that matched its ribbon-shaped retina. We also found that lens angular resolution increased with depth. Due to a similar trend in the angular separation between adjacent ganglion cells in the retinas of fishes, the perceived visual contrast at the retinal cutoff frequency was constant with depth. The increase in acuity with depth allows the predators to focus all the available light bioluminescent prey animals emit and detect their next meal.

Optical advantages and function of multifocal spherical fish lenses.

The spherical crystalline lenses in the eyes of many fish species are well-suited models for studies on how natural selection has influenced the evolution of the optical system. Many of these lenses exhibit multiple focal lengths when illuminated with monochromatic light. Similar multifocality is present in a majority of vertebrate eyes, and it is assumed to compensate for the defocusing effect of longitudinal chromatic aberration. In order to identify potential optical advantages of multifocal lenses, we studied their information transfer capacity by computer modeling. We investigated four lens types: the lens of Astatotilapia burtoni, an African cichlid fish species, an equivalent monofocal lens, and two artificial multifocal lenses. These lenses were combined with three detector arrays of different spectral properties: the cone photoreceptor system of A. burtoni and two artificial arrays. The optical properties compared between the lenses were longitudinal spherical aberration curves, point spread functions, modulation transfer functions, and imaging characteristics. The multifocal lenses had a better balance between spatial and spectral information than the monofocal lenses. Additionally, the lens and detector array had to be matched to each other for optimal function.

Nocturnal homing: learning walks in a wandering spider?

Homing by the nocturnal Namib Desert spider Leucorchestris arenicola (Araneae: Sparassidae) is comparable to homing in diurnal bees, wasps and ants in terms of path length and layout. The spiders' homing is based on vision but their basic navigational strategy is unclear. Diurnal homing insects use memorised views of their home in snapshot matching strategies. The insects learn the visual scenery identifying their nest location during learning flights (e.g. bees and wasps) or walks (ants). These learning flights and walks are stereotyped movement patterns clearly different from other movement behaviours. If the visual homing of L. arenicola is also based on an image matching strategy they are likely to exhibit learning walks similar to diurnal insects. To explore this possibility we recorded departures of spiders from a new burrow in an unfamiliar area with infrared cameras and analysed their paths using computer tracking techniques. We found that L. arenicola performs distinct stereotyped movement patterns during the first part of their departures in an unfamiliar area and that they seem to learn the appearance of their home during these movement patterns. We conclude that the spiders perform learning walks and this strongly suggests that L. arenicola uses a visual memory of the burrow location when homing.