1909 | Heidelberg, Germany

Sea urchin (Echinoidea) debris wearing

If you spend enough time digging into animal behaviour, you’ll eventually run into the umwelt. In its broadest meaning the term is German for ‘environment’. But it has also picked up a narrower, ecological meaning: the subjective world that centres on a given creature, based on its own unique set of senses. Everything that an animal can experience makes up its umwelt, and everything else just doesn’t exist for that animal.

Humans have our own umwelt, which includes for example the narrow bands of light and sound we can see and hear, but doesn’t include infrared (heat) detection, or a strong sense of the Earth’s magnetic field, or the ability to detect and interpret electrical signals. An umwelt is actually a valuable guide to what really matters to a given species, since evolution tends to trim away any unnecessary abilities.

This conception of a self-world was introduced over a century ago by Estonian-born aristocrat and biologist Jakob von Uexküll, and his ideas continue to resonate. For instance, the excellent recent book on animal senses by Ed Yong, An Immense World, explores in depth numerous umwelten and the hidden (to us) universes they reveal. But today we’re following Uexküll for a slightly different reason: his early fascination with sea urchins.

The hedgehog’s hat

Uexküll personally experimented with several species of what he called seeigel. In German this translates literally to ‘sea hedgehog’, which makes sense when you see these spiny little critters gathered across the sea floor (although land hedgehogs never seem to hang out in their thousands as sea urchins can do). Uexküll was interested in their reactions to external prompts, as part of building up an idea of how the world appears to them.

He spent a lot of time exposing sea urchins to degrees of light and shade, finally concluding that the animals were responding to any form of moving shadow, no matter the cause. That makes sense when the shadow is a possible predator, but it also left the sea urchins taking a defensive posture to passing clouds, or boats. This is how Uexküll represented their behaviour:

The top panel is the real world of objects near and far, the sea urchin’s umgebung or vicinity as Uexküll labels it. The bottom panel is what the sea urchin perceives: an umwelt of hovering shady characters, towards any one of which it presents a spiny front.

The image is from Uexküll’s 1934 co-authored book Streifztige durch die Umwelten von Tieren und Menschen: Ein Bilderbuch unsichtbarer Welten, or ‘A stroll through the environments of animals and people: a picture book of invisible worlds’. By that point he had been working on the light responses of sea urchins for decades, starting in the 1890s at a research station in Naples.

He found that various species reacted differently to shifting light—some would run away, some would shield themselves using their spines. Others would take a more proactive stance, using nearby debris as tools. Translated from his 1909 book that introduced the umwelt:

The exposed spines carry out movements in very irritable species. The other species of sea urchins are content with a slow escape movement or they at least transport the objects that burden their spines, be it stones or algae leaves, towards the illuminated area, and in this way create a screen of light.

Here’s an example of a blunt or purple sea urchin (Sphaerechinus granularis) that’s so covered itself in stones it’s barely visible:

Uexküll understood that his Italian seeigels were deliberately collecting and moving objects onto their upper body as a way of dealing with changing external cues, clutching on to their tools with tiny tube feet or podia. And his conclusion that these tools were essentially shade umbrellas has been since confirmed in other parts of the world. For example, experiments in Jamaica in the 1950s found that the urchin Lytechinus variegatus covered itself within five minutes of exposure to light, and usually dropped its umbrellas after a few hours of darkness. If the direction of the light source moved, the sea urchin would slowly shift its cover to block that new direction.

Norman Millott, who did that Jamaican work, provided a handy diagram showing how the tube feet use suction to first draw in an object, then assist with leverage from the spines to work it up onto the body (spines above the object flatten out to help the processes). In the picture the urchin, on the right and missing most of its spines for illustrative reasons, is pulling in and then positioning a gastropod shell:

Not drowning, waving

Although many sea urchins have an aversion to light—they are ‘negatively phototactic’—not all show such a dramatic tendency to cover themselves. In the time since Uexküll’s work, therefore, additional hypotheses for the covering behaviour have emerged and are still being tested.

For example, in 2019 Glyn Barrett of the University of Reading led a team that reported on the behaviour of four sea urchin species in the Philippines. They were interested in comparing UV exposure of their test subjects with other possible reasons for covering, such as ballast to stay steady during strong waves or camouflaging their scent. The scientists were also curious about whether the animals were selecting specific types of covering material, or just randomly picking up junk. The urchins in their study all lived in fairly shallow island waters, 2 to 16 metres deep, and all showed some degree of natural object wearing.

Here’s one of their targets, Tripneustes gratilla, hanging out in fashionable seaweed and shell drapery:

The study’s first conclusion was that there really are fashion trends. The smallest of the species, Salmacis sphaeroides, was more into softer seagrass coverings than the others, while the largest, Toxopneustes pileolus, had a preference for hard coral and shells. The team also discovered that the urchins worked relatively quickly for animals that can often seem immobile at first glance. If deprived of their current material, they grabbed new pieces and dragged them in at a rate of 1-2cm per minute.

We can use the Philippines work to look more closely at the process of holding and moving that debris. In the photos below, (A) shows the stretching podia with their little suction cups attached to some coral rubble, while (C) gives us a look at the spines supporting and pushing a fragment upwards onto the animal (these are T. gratilla again):

The researchers didn't find much of an effect of wave power on three of their study species, but for one—the large T. pileolus—the amount of material it carried got less and less as the water got deeper. That’s consistent with both a need for more UV protection at the surface, as well as a need for more stability for shallow water dwellers, where the waves are most intense. The report notes that sea urchins of other species living below the range explored in this study might show similar current-related shifts in which tools they use.

However, urchin behaviour at depth might instead be even stranger. For instance, sea urchins of the genus Echinus living more than a kilometre down in the cold ocean still cover themselves with algae. There, sunlight and wave action aren’t factors, so exactly what are these critters doing? One hypothesis is that they are wearing edible clothing, carrying species that are part of their diet. Hoever, their algae hats might also help them camouflage, cosplaying as algae lumps instead of tasty urchins. As usual, and especially for research in the deep ocean, more work is needed to nail down the relative importance of these influences.

Comparing family relationships between sea urchin species shows that covering doesn’t follow neat patterns, with large portions of the family tree devoid of species that show this behaviour. This means that it has re-evolved multiple times throughout this widespread group, and therefore we should expect to find different reasons for animals in different circumstances. Sunlight matters, and it’s something we can track and experiment with, but what we really need to pay attention to is what the animal itself sees and feels: its umwelt.

Music of the spheroids

Jakob von Uexküll was fond of using musical metaphors for his insights into how animals assign meaning to their world. To him, life was a symphony, and signals such as a sea urchin detecting a shadow were like bells or a violin ringing out through the creature’s umwelt.

This perspective led him to quite poetic if convoluted statements. For example, from his 1940 book Bedeutungslehre (The Theory of Meaning):

Only with the demonstration provided by Driesch that a sea urchin germ cell cut in half became not two halves, but two whole sea urchins of half the size, opened the way for a deeper understanding of the technology of Nature. Everything physical can be cut with a knife—but not a melody. The melody of a song played on a free carillon of living bells remains unchanged, even if it only controls half the number of bells.

Uexküll’s point was that there is more to biology than the physical matter that makes it up; there is also meaning/melody. As humans continue to add more and more noise into the environment, we are changing the meaning of the world, the umwelt, of every creature we blunder into. Some will be unable to cope, as our light pollution, sound pollution and atmospheric pollution cut them off from their evolved environments.

And some, like this sea urchin, might literally take it all in their stride, and make the best of whatever pollution we throw their way:

Sources: Uexküll, J. (1909) Umwelt und Innenwelt der Tiere. Berlin, Verlag von Julius Springer. || Uexküll, J. & G. Kriszat (1934) Streifzüge durch die Umwelten von Tieren und Menschen: Ein Bilderbuch unsichtbarer Welten. Berlin, Verlag von Julius Springer. || Vafidis, D. et al. (2020) Population Density, Size Structure, and Reproductive Cycle of the Comestible Sea Urchin Sphaerechinus granularis (Echinodermata: Echinoidea) in the Pagasitikos Gulf (Aegean Sea). Animals 10:1506. || Millott, N. (1955a) The Covering Reaction in a Tropical Sea Urchin. Nature 175:561. || Millott, N. (1955b) The Covering Reaction of Sea-Urchins: I. A Preliminary Account Of Covering in the Tropical Echinoid Lytechinus variegatus (Lamarck), and its Relation to Light. Journal of Experimental Biology 33:508-523. || Barrett, G. et al. (2019) Tool Use by Four Species of Indo-Pacific Sea Urchins. Journal of Marine Science and Engineering doi:10.3390/jmse7030069. || Ziegenhorn, M. (2017) Sea Urchin Covering Behavior: A Comparative Review. In M. Agnello (ed.) Sea Urchin - From Environment to Aquaculture and Biomedicine. IntechOpen. || Uexküll, J. (1940) Bedeutungslehre. Leipzig, Barth.

Main image credit: Emilie Novaczek; http://www.backtothesea.org/blog/guest-post-urchins-wearing-hats || Second image credit: Uexküll (1934) || Third image credit: Alexios Lolas, in Vafidis et al. (2020) || Fourth image credit: Millott (1955b) Fig. 1 || Fifth image credit: Rich Mooi, California Academy of Sciences || Sixth image credit: Barrett et al. (2019) Fig. 7 || Seventh image credit: Michael Patrick O'Neill