Box jellyfish stable-eyes vision to hunt prey


Ernst Haeckel's Kunstformen der Natur (Artforms of Nature) was a landmark in biological illustration. Published in 1904, it was lavishly illustrated with 100 exquisitely detailed lithographic plates, including this one, showing nine different species of cubomedusae, or box jellyfish.

It has been known, since around the time that Haeckel's masterpiece was published, that box jellyfish have a unique visual system which is more sophisticated than that of other jellyfish species. They boast an impressive set of 24 eyes of four different types, which are clustered within bizarre sensory appendages that dangle from the cube-shaped umbrella. The known light-guided behaviours of these organisms are, however, relatively simple, so exactly why they possess such an elaborate array of eyes was somewhat puzzling.

A group of Scandinavian researchers working in the Carribean now report that one of the box jelly's eye types is highly specialized to peer up towards the water surface at all times, so that it can use terrestrial landmarks to navigate towards its prey.

Anders Garm and his colleagues have been conducting experiments on wild populations of Tripedalia cystophora, a box jelly that inhabits the mangrove lagoons near La Parguera in Puerto Rico. These organisms, which measure just 10mm in diameter, inhabit the shallow water near the edges of the lagoons, between the prop roots of the mangrove trees. Here, they stay close to the water surface, where their prey - small crustaceans called copepods - gather in large numbers in the shafts of light formed by gaps in the mangrove canopy above.

Like other box jellys, T. cystophora has 24 eyes contained within a club-shaped sensory apparatus called a rhopalium, one of which is suspended from each side of the cube-shaped umbrella by a flexible, muscular stalk. Each rhopalium contains a cluster of six eyes - one pair of slit eyes, one pair of pit eyes, one lower lens eye and one upper lens eye. The slit eyes and pit eyes are simple structures consisting of openings containing light-sensitive pigments. The lower and upper lens eyes are 'true' eyes which resemble those of cephalopods and vertebrates more closely than those of other jellyfish. They contain a spherical lens, iris, cornea, which together work like a camera to form an image onto photoreceptor cells in the retina.

Garm and his colleagues are interested in how eyes evolved, and how they are adapted to an animal's lifestyle and habitat. Several years ago, they showed that box jellys use vision to avoid obstacles that might damage their delicate bodies, and that this avoidance response differs between species - it is stronger in T. cystophora, which is usually surrounded by roots, than in Chiropsella bronzie, which lives in shallow water off the sandy beaches of Queensland, Australia, a habitat that contains few obstacles.

Garm's group had also observed that T. cystophora quickly swim back to the edge of the lagoon when moved away from it. This behaviour is essential for survival - they forage for food at the lagoon's edge, and risk starvation if they stray too far. The researchers speculated that they might use the upper lens eye to navigate toward the edge of the lagoon, and performed a series of behavioural experiments to test the idea.

They placed a clear tank with cylindrical walls and a flat bottom in the water under the mangrove canopy, and filled it with water so that it floated, with the walls extending several centimenters above the water surface. They then placed a group of jellyfish in the tank and slowly dragged it away from the lagoon's edge, and recorded the movements of the jellyfish with a video camera suspended beneath the tank.

Using a geometrical model they had developed previously, the researchers predicted how the resolution of the eye would limit the detection of the mangrove canopy. At 5m tall, the mangrove trees would be detected easily at distances of 4m, but detection would be more difficult at 8m, due to ripples on the water surface, and impossible at 12m. This is exactly what was found in the behavioural experiments.

The jellyfish were seen to swim along the edges of the tank, bumping into it constantly as it was moved. But rather than swimming randomly, they always swam in the direction of the nearest mangrove trees. This behaviour was most evident when the tank was between 2 and 4 meters away from the lagoon edge. The jellyfish could still detect the direction of the nearest trees from a distance of 8 meters, but swam randomly along the edge of the tank when it was 12 meters or more away.

The experimental tank sealed off the water surrounding the jellyfish inside it, so that they could not detect any chemical cues in their environment, or the mechanical forces that would normally generated by movement. Visibility in the lagoon is poor, and there are no recognizable underwater landmarks. And the finding that their navigational ability depends on distance rules out the possibility that they use cues from the sun. So the only remaining explanation is that they are using the upper lens eye to detect visual cues from the mangrove canopy, and use these cues to determine the direction of the nearest lagoon edge. This was confirmed by a further experiment, in which a white sheet was used to obscure the canopy - with the trees hidden from view, the jellyfish swam randomly.

box jellyfish eyes.jpg

Close-up video recordings of freely-swimming T. cystophora revealed that the upper lens eye is remarkably specialized for this behaviour. Each rhopalium contains a heavy crystal called a statolith, which is found at the end of the muscular stalk furthest from the body. These weigh down the rhopalia, causing the stalk to bend when the jellyfish changes the orientation of its body.

Consequently, the upper lens eyes remain in a strictly upright position, regardless of body orientation (above), and their visual fields point directly upwards, even when the jellyfish is completely upside-down. The lower lens eyes, on the other hand, which are thought to be be required for repulsion and attraction to underwater objects, always point downwards.

The researchers used their geometric model to investigate the optical properties of the upper lens eye, revealing another remarkable specialization. Water bends light waves entering it, causing the 180° visual field we are accustomed to be compressed. From beneath the surface, everything above is seen through a cone of light with a width of about 96°. According to the researchers' simulation, the visual field of the upper lens eyes has a width of between 95° and 100°. This further suggests that the upper lens eyes probably evolved for the sole purpose of detecting visual cues from above the water surface.   

The use of terrestrial landmarks for navigation is an advanced visually-guided behaviour, and this is the first time that such behaviour has been observed in a jellyfish species. The box jelly nervous system is more highly developed than that of other jellyfish, but nevertheless lacks a brain, and consists of a nerve ring around the base of the umbrella. The findings therefore show that a centralized brain is not necessary for advanced behaviours.

Navigation is the only known purpose of the upper lens eyes; similarly, the purpose of the lower lens eyes is apparently restricted to detection of underwater objects. Eyes like these, which support a single visually-guided behaviour, represent an early stage in the evolution of visual systems, and are presumed to require less neural processing power than multi-purpose eyes such as ours.

The complex eye arrays may, therefore, be an evolutionary strategy for producing complex visually-guided behaviours in the absence of a brain, and could explain why the box jelly nervous system is more complex than that of other jellyfish species. It is, however, unclear how box jellys process visual information, and this is something that Garm's group is keen to explore.

Garm, A., et al. (2011). Box Jellyfish Use Terrestrial Visual Cues for Navigation. Curr. Biol. DOI: 10.1016/j.cub.2011.03.05

Garm, A., et al. (2007). Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J. Exp. Biol. 210: 3616-3623 [PDF]

Nilsson, D. E., et al. (2005). Advanced optics in a jellyfish eye. Nature 435: 201-205 [PDF]


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It seems that the eye structures you detail are similar to the ones in our own inner ear! They determine the jelly's orientation and balance in the water, and use it as direct feedback for the jelly to orient itself and avoid harm.

One hesitates, however, to call the jellyfish "without a brain". Perhaps its nervous system disseminated acts like a brain in toto, as we have a "brain in our gut" to help us make decisions. Even if there is no centralized body present, the neurons and perhaps the eyes themselves ARE the brain, much like distributed computing.

Just a thought. Thanks for a very interesting post.

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