I’m surprised that I haven’t gotten around to posting this yet. Here is one of my favorite mantis shrimp videos of all time.
This segment was a bit of humor produced for ‘The Fastest Claw in the West,’ a documentary from 1985 about mantis shrimp. It is narrated by blog-hero David Attenborough, and features stomatopod expert Roy Caldwell. It turns out you can watch the whole thing on Youtube. It’s great fun and very informative. I highly recommend it:
The rather amusing cover of this month’s JEB caught my eye; I am always excited to find out about the outlandish and creative methods that scientists dream up in order to test their ideas.
SCIENCE!
Yep, that’s a jumping spider holding a styrofoam ball, tethered to the ceiling. So what the heck could possibly be going on here?
The cover shot belongs to this paper. The researchers wanted to get a better handle on the contributions of specific jumping spider eye sets to the animal’s overall visual perception and behavior. Like many arachnids, jumping spiders have eight corneal eyes. Two sets of these eyes are forward facing; the anterior median (AM) and anterior lateral (AL) eyes (see image below). The large set of AM eyes are extremely acute, boasting the highest known resolution among the arthropods. However, they have an extremely narrow field of view since their retina is organized into a thin strip, not unlike the ribbon retina of larval diving beetles. The AL eyes, on the other hand, have a much larger, overlapping field of view and are very good at detecting movement. When the spider detects something with the AL eyes, it reorients its body to bring the high-resolution AM eyes to bear on the target. When jumping spiders are active they can be seen constantly preforming these reorienting body movements, endowing them with a great deal of inquisitive charm and personality (adorable videos).
Anterior median (AM) and anterior lateral (AL) eyes of Maevia inclemens. Photo: Thomas Shahan
Now, back to the recently published study. The researchers wanted to assess the importance of the AL eyes in the orientation response of jumping spiders. They used an opaque silicone paint to block out all the animal’s eyes besides the two AL eyes. They then tethered the jumping spiders from above using a piece of cork and beeswax. Finally they ‘handed’ the spiders a gridded polystyrene sphere (which they readily accepted), and positioned them in front of computer LCD monitors. Varying dot stimuli were displayed on the monitors, and the orientation response of the spiders to these stimuli were easily recorded by observing the underfoot movements of the polystyrene sphere.
The researchers found that the jumping spider’s AL eyes are crucial to orientation responses, and therefore extremely important to the spider’s visual ecology. In fact, the spiders in this study demonstrated complete hunting behaviors using only the AL eyes. In addition, the researchers noted that increased hunger yielded stronger predatory response in the jumping spiders. Finally, they observed that overall, females showed a greater orientation response to stimuli than males. The researchers suggest that this is due to visual dimorphism, possibly related to the female’s need to carefully scrutinize the courting displays preformed by males.
So, that’s why the cover of JEB is a photo of a hanging jumping spider holding a polystyrene ball. However, the best part of this outlandish-seeming experiment is that the tests were non-destructive. The paint covering the eyes, and the tether attached to the back, could be removed without harming the jumping spiders. They were, unfortunately, eventually forced to give up their toy ball.
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References:
Zurek, D., Taylor, A., Evans, C., & Nelson, X. (2010). The role of the anterior lateral eyes in the vision-based behaviour of jumping spiders. Journal of Experimental Biology, 213 (14), 2372-2378 DOI: 10.1242/jeb.042382
Go look at more of Thomas Shahan’s unbelievable photography, here.
Mantis shrimp use a variety of visual signals in order to communicate with one another. One set of commonly used signaling structures are the antennal scales; flattened, paddle-like structures derived from the second antennae and set on either side of the mantis shrimp’s head. They have a wide range of motion and can be directed at other mantis shrimp as part of intraspecific threat and mating displays. The antennal scales are often adorned with attention grabbing color and polarization patterns that stand out to other visually adept mantis shrimp.
Attenuation of light in water. Adapted from Levine and MacNichol, 1982
However, the deep ocean is not kind to color contrast. As you move deeper, the absorptive and refractive properties of water attenuate the spectrum of available light. Longer and shorter wavelengths are filtered out until eventually the only available light is blue-green, around 480 nanometers in wavelength (left). Despite this limitation, some deep water mantis shrimp have found a way to preserve their color signals in an essentially monochromatic environment.
Lysiosquillina glabriuscula has bright yellow spots on its antennal scales and the underside of its carapace. This species is found in the shallows as well as at greater depths. It turns out that the yellow spots contain fluorescent materials that are stimulated by blue light and emit yellow light, similar to the yellow reflected light that the spots produce in white lighting. Therefore, these mantis shrimp are able to preserve their yellow spot signals at depths where there is only blue light available.
L. glabriuscula in white light (left) and blue light (right). Blue light is filtered out in the second picture in order to better show the green and yellow fluorescence on the animal. Adapted from Mazel et al., 2004
References:
Mazel CH, Cronin TW, Caldwell RL, & Marshall NJ (2004). Fluorescent enhancement of signaling in a mantis shrimp. Science (New York, N.Y.), 303 (5654) PMID: 14615546
The sunburst diving beetle, Thermonectus marmoratus, is an adept predator. As adults, these Dytiscid beetles are strong swimmers and prey on a variety of aquatic animals by tearing them to shreds with their powerful mandibles. They also spend some time out of water and can fly from one water supply to another. When it is time to reproduce, female diving beetles enter the water and lay eggs on the stems of aquatic plants and macroalgae. When the eggs hatch, the larvae (known commonly as water tigers) enter the water column and begin their rein of terror.
In the lab, these morphologically distinct diving beetle larvae are typically fed tadpoles or mosquito larvae. In the wild, however, they probably eat anything unlucky enough to get too close. When hunting, these beetle larvae either swim around actively or hang, with their tail touching the surface, just below the water line. When they spot a prey animal, they swim over and strike the target with their powerful mandibles (Watch a video of a predation event below). Unlike the adults, larval diving beetles gradually suck the fluids from their prey, resulting in an unfortunately slow demise.
The predatory nature of sunburst diving beetle larvae is highly dependent on their visual system; and boy is it a bizarre one. While the adults have typical arthropod compound eyes, the larvae see the world through stemmata. Stemmata, which are commonly seen in larval insects, are simple lens eyes that rely on superficially similar optical principles to vertebrate eyes. On each side of the head, the larvae have six stemmata as well as a lens-less eye patch (see below). Within each of these eyes there are two distinct retinas, one on top of another. In total, this means that these T. marmoratus larvae have fourteen eyes and twenty-eight distinct retinas!
Front and side views of the head of a T. marmoratus larva. E, eye; EP, eye patch; M, mandible. Adapted from Mandapaka et al., 2006 and Maksimovic et al., 2009.
This larval visual system has a befuddling number of bizarre optical properties. The retinas are sensitive to a broad range of wavelengths, including UV, and the photoreceptor architecture is suggestive of polarization detection. In addition, some of the lenses seem to have novel bifocal and chromatic aberration-correcting properties. Despite the research into all of these strange visual adaptations, the ecological significance of most of the eyes on this animal is completely unknown.
The best understood eyes in the diving beetle larva are E1 and E2. They are forward-looking and primarily used for predation. However, when you look at the main retina in these eyes, you surprisingly find that it is only composed of a thin horizontal band, two photoreceptors tall. Imagine trying to view the world in a thin strip, two pixels high! So, how is the diving beetle larva using these eyes to zero in on prey? Well, it turns out that these sort of strip eyes are not completely novel in nature. Jumping spiders, some copepods, and a pelagic snail all have strip retinas. In order to see the world, they scan their narrow retinas rapidly back and forth, as in the image below. Diving beetles, on the other hand, have absolutely no musculature to move their eyes or retinas. So how do they see?
Look again at the predation video from above. Notice that once the diving beetle larva spots the mosquito larva, it begins bobbing its entire head up and down. The diving beetle larva is scanning the mosquito with the strip retina in its main eyes. As it gets closer, the scanning movement actually becomes more pronounced, since the target takes up more of the field of view. This technique allows the diving beetle larva to accurately hone in on its prey without sacrificing limited head-space for a full retina or eye muscles.
The closer you examine arthropods, the weirder they seem to get. Who would have though that this small aquatic predator would have such a complex and fascinating visual system? In order to discover the most exciting aspects of living things, you need to look. That’s where science starts; with someone peering through the confounding subterfuge of nature, hoping to widen our glimpse of the gear-works within.
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The research discussed in this post is being carried out at Buschbeck lab at the U. of Cincinnati.
References:
Mandapaka K, Morgan RC, & Buschbeck EK (2006). Twenty-eight retinas but only twelve eyes: an anatomical analysis of the larval visual system of the diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae). The Journal of comparative neurology, 497 (2), 166-81 PMID: 16705677
Buschbeck EK, Sbita SJ, & Morgan RC (2007). Scanning behavior by larvae of the predacious diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae) enlarges visual field prior to prey capture. Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology, 193 (9), 973-82 PMID: 17639412
I haven’t been able to post any hard science this week since I’ve been working on a presentation for my department’s annual symposium. So far, this is the largest audience I have presented my work to.
I thought I might quickly share one of my slides from that presentation as a preview for a much larger future post about the ridiculously complicated mantis shrimp visual system.
Click to embiggen. Stomatopod Photo: Roy Caldwell
This is a comparison of photoreceptor classes in human and mantis shrimp retinas. Each photoreceptor class has a distinct wavelength sensitivity curve. On the human plot, you can see our three cone photoreceptor classes; blue, green, and red. These receptors cover the electromagnetic light spectrum between 400 nm (violet) and 700 nm (red). Our brains are able to process relative stimulation between the three cone photoreceptor classes, allowing us to differentiate many colors.
Mantis Shrimp don’t have the advantage of a large brain for downstream processing, so they take another approach to seeing many colors: They have 16 distinct photoreceptor classes, packed via optical filtering into tight slivers of the spectrum. Of these, five classes are sensitive to UV light, below our visual range (these are the receptor classes that I am attempting to characterize). In addition, not shown in this slide, mantis shrimp can discriminate linearly and circularly polarized light.
Stay tuned for an in depth mantis shrimp vision post at some point.
PBS has a great video up about the evolution of camera eyes, from their documentary, Evolution: ‘Darwin’s Dangerous Idea’. Using a synthetic optical demonstration and examples from nature, Dan-Eric Nilsson describes some of the selectable gradations between a flat patch of photosensitive cells and a fully functional camera eye. Camera eyes, also called simple lens eyes, have a single chamber with a light-sensitive retina on one wall, across from a lens, through which light enters and is focused onto the retina.
Dan-Eric Nilsson holding the lenses of a collossal squid. Photo: Museum of NZ, Te Papa.
Camera eyes are found in most vertebrates; the only exceptions being species that have regressively lost their eyes due to low-light lifestyles. There are other examples of camera eyes in nature, however. The best know among these are cephalopods. Octopus, squid, and cuttlefish all have camera-style eyes that are structurally very similar to vertebrate eyes. This is a classic example of convergent evolution: Despite independent retinal derivation, vertebrates and cephalopods have both hit on a similar eye design solution for seeing their world. There are further examples of lens eyes in jellyfish, annelid worms, and gastropod mollusks; also typifying the concept of convergent evolution.
Less commonly known is that some arthropods have also discovered simple camera eyes. The majority of arthropods have compound eyes, composed of many independent optical units called ommatidia. Each ommatidial facet of a fly’s eye, for example, has its own lens and photoreceptor apparatus. Compound eyes work very well for most arthropods, however their maximum resolution is limited by their structure: The smaller the lens, the greater the light diffraction anomalies it produces; and compound eyes require thousands of very small lenses. Therefore, some arthropods have evolved camera-like simple eyes, with a single chamber in order to greatly increase resolution.
Arachnids, and specifically jumping spiders, possess the prime examples of simple eyes among the arthropods. They make use of a corneal simple eye. In a corneal simple eye there is no crystalline lens and the refractive focusing of light is carried out solely by the curved cornea. Using simple corneal eyes, jumping spiders achieve the greatest visual resolution among arthropods. In addition, some tiny copepod crustaceans have been found to have simple eyes with lenses. Among these, certain genera even have multiple lenses, producing telescoping optics.
Simple camera eyes are a spectacular example of convergent evolution. They can be found in at least five of the major animal phyla; Cnidaria (jellies), Arthropoda, Chordata (including vertebrates), Annelida (worms), and Mollusca. These phlya represent a tremendous diversity of creatures separated by vast eons of deep evolutionary time. This demonstrates the ability of a useful design to reveal itself through evolution in disparate lineages; built from whatever components are available.
References:
LAND, M. (2005). The optical structures of animal eyes Current Biology, 15 (9) DOI: 10.1016/j.cub.2005.04.041
New research published in the Journal of Experimental Biology sheds light onto visual stimuli processing in arthropods. Researchers (Avargues-Weber et al., 2010) have shown that honeybees, Apis mellifera, are capable of complex visual processing and learning tasks that are commonly reserved for primates. With a small fraction of mammalian neural complexity, honeybees are capable of discriminating face-like visual stimuli; both between face-like and non-face-like stimuli and between variations of face like stimuli. That is, the honeybees are capable of visually discriminating and remembering one human face from another.
Of course, there is no ecological reasoning for honeybees to discriminate human faces, but the behavior is a clue about the bee’s underlying visual processing capacities. This research tells us that honeybees are able to perceive and learn, not just the individual components of a visual stimulus, but the interrelationships between them. This is the first demonstrated instance of configural processing in an arthropod.
Members of this research team first suggested that bees were capable of discriminating human faces in 2005. However, their work was criticized because it did not control for low-level stimuli (individual cues, center of gravity, symmetry, spacial frequency, and background cues) in the faces. That is, the researchers did not clearly show that the bees were actually carrying out configural processing; perceiving the interrelationships of multiple facial components processed together.
In their new paper, the researchers preformed a variety of behavioral experiments to control for low-level visual cues. They primarily used a Y-maze chamber with a choice of two visual stimuli at the end of the two branches. The bees were trained to associate a sugar reward with one of the stimuli. Afterwords, in the absence of a reward, the researchers recorded the percentage of correct choices by the bees.
First, the researchers showed that the bees could distinguish face-like and non-face-like arrangements of dashes and dots. Furthermore, they confirmed that the bees were discriminating based on the combined relationship of the eyes, nose, and mouth components of the face-like arrangements; and not just the orientation of individual components. A series of additional controls showed that the bees were not using symmetry, center of gravity, or spatial frequency cues to distinguish the stimuli. Finally, the researchers showed that the honeybees could also distinguish photos of human faces. Some of the choices that the honeybees were able to distinguish.
This research concludes that honeybees are capable of high-level cue integration and configural visual processing. Such a capacity in honeybees is likely used for navigation and identifying flowers. The neurobiology responsible for configural visual processing is only partially understood in humans, and completely undescribed in arthropods. By working out this processing system in comparatively simple insect brains, researchers can hope to eventually apply this finding to synthetic facial recognition systems.
References:
Avargues-Weber, A., Portelli, G., Benard, J., Dyer, A., & Giurfa, M. (2010). Configural processing enables discrimination and categorization of face-like stimuli in honeybees Journal of Experimental Biology, 213 (4), 593-601 DOI: 10.1242/jeb.039263
Polarized light is tough for us to comprehend. It’s all around us, but we cannot see it without the aid of technology (Actually, that is not quite true. There is an extremely weak visual phenomenon known as Haidinger’s brush which is the extent of polarization perception in humans. I actually had not been able to see the effect until writing this article).
Regardless, our meager polarization perception is the exception rather than the rule in the animal kingdom. Whereas Haidinger’s brush is a useless side-effect of the optics in our eyes, other animals use polarized light vision for navigation, communication, and contrast-enhancement. It can be thought of as an additional channel of visual perception, akin to color vision. We are functionally polarization-blind. Arthropods on the other hand, are masters of perceiving the polarized world.
Arthropoda 
