2019 | Ile aux Aigrettes, Mauritius

Sponge crab (Alcockdromia fallax) algae carrying

Imagine: it’s really wet outside. You desperately need an umbrella, but all you can find is an old shower curtain. Going out uncovered isn’t an option, so you resign yourself and quickly snip out a section from the curtain, big enough to cover your body. Then, holding it carefully above you, you head out into the storm.

It’s a classic tale of human ingenuity and technology: you recognise a problem, find a solution that makes the best of what you’ve got, and go about your day with added security. But what if we changed the picture a little, scaled you down to a fraction of your normal size, and moved the action to a shallow seabed in the Indian Ocean, somewhere off the coast of Mauritius? Oh, and what if we gave you ten legs, an exoskeleton, and bulbous eyes? In short, what if you were a crab?

In this post we’ll explore the extraordinary world of carrying crabs, animals that not only actively use tools for protection, but can make those tools when needed. And we’ll find evidence that they’ve been doing this for so long, they’re one of the few animals ever to evolve special body modifications to assist with their tool use.

Hidden intentions

To begin, let’s re-cast the above scenario in terms a sponge crab would recognise. It’s a given that it’s wet outside—your natural habitat is a shallow lagoon, or maybe a rock pool intermittently exposed by the tide. Umbrellas aren’t much use underwater, and besides, it’s not really protection from the weather that bothers you. What you need is a covering that shelters you from something that might eat you.

That bit about the shower curtain isn’t so far off, though. You’re surrounded by seaweed and algae of all shapes and sizes, including flat sheets of brown bracket alga (Lobophora variegata) and green sea lettuce (Ulva lactuca). Both of these grow as flattened plates or leaves. And you have one advantage over the humans: you’ve got scissors for hands. Your pincers can easily cut out a piece just the right size to cover you, leaving one natural edge intact.

From there, you just crawl under your algae sheet, and voila! you’re hidden. And quite cosy—just look again at the image at the top of this post. But…you can’t go anywhere. And surely that sheet will blow away with the current.

Wouldn’t it be great if you could somehow keep a tight grip on the sheet over your back, while still strutting around the ocean floor in your stylish greenish-brown overcoat? Welcome to the stage, evolution.

Several related families in the infraorder Brachyura—known as the ‘true’ crabs to distinguish them from other crab-like animals such as hermit crabs and horseshoe crabs—have developed an odd twist to their back legs. It’s literally a twist: the final one or two pairs of legs sit above the animal, instead of beneath it, where legs are supposed to be. (If you’re into your crab anatomy, these are pereiopods or walking legs, not the swimming pleopods found further back on the animal.)

From this elevated position, the legs can grasp things and position them over the body—that umbrella part of our original analogy makes more sense here. Among the various crab families, these dorsal or ‘back’ legs are often shrunken, and also can have numerous types of hooks, pincers, feelers or other appendages to help latch onto whatever covering is needed.

The Mauritian crabs we’ve been looking at so far—Alcockdromia fallax, named by New Zealand marine biologist Colin McLay—are in fact rather unusual in their choice of coat material, and in their level of tool manufacture. The world of carrying crabs literally goes much deeper. But you can see those cleverly evolved dorsal legs in the photo above, raising the piece of cut sea lettuce, undamaged edge facing forward, in a stance that McLay describes as

looking remarkably like a paraglider about to launch from a hill-top.

McLay also was the first to describe Desmodromia tranterae, a roughly 1cm square crab found in coastal Western Australia. A male of the species collected in 1999 near Murujuga—or the Burrup Peninsula—was carrying around a bivalve shell more than twice its width and length. In the accompanying front-on photo you can see its fifth legs tucked up on its back, as well as how the crab looked from underneath, when securely holding on via the bivalve’s hinge:

The anatomical adaptations that allow crabs to carry things around (including highly mobile joints on those raised legs, just like our own highly mobile shoulder joint) likely go back as far as the Late Jurassic or subsequent Cretaceous periods. That’s well over 100 million years, far longer than the few million years that humans have walked upright, or had supercharged brains or opposable thumbs. It’s not an exaggeration to say that, since the time of the dinosaurs, crabs have been among the dominant tool users on Earth.

Who wore it best?

The fact that these Brachyuran crabs actively select, modify, grasp and manipulate their coverings as they travel around makes this undisputed tool-use. It is not simply debris falling on or randomly sticking to a crab’s back, a process that does happen and is known as epibiosis. Veteran crab-ologists Danièle Guinot (of the French Muséum national d'Histoire naturelle) and Mary Wicksten (of Texas A&M University) are emphatic about crab tailoring:

Living sponges are carefully chosen, cut, and modelled to perfectly fit the crab’s body without covering the eyes or mouthparts.

If this kind of thing was happening with larger animals, especially on land where we humans more regularly encountered them, it would be held up as a prime example of animal technology. Just imagine if a lioness used her claws to tear a buffalo hide into a cloak that she then wore while slinking through the tall grass, or if emus made a bark shelter to carry on their back as they ran under the sweltering Australian sun. Everyone would know about that.

As we wander through the world of animal tool use, it therefore helps to remind ourselves that an awful lot of what animals can do is either unknown or ignored by most of us. Their behaviour may also look different from what we expect, because not all animals have hands, or a face, or teeth, or skin. It’s much easier for us to imagine ourselves in the position of a monkey or ape. But if we want to truly understand what (if anything) separates human technology from the rest of the natural world, we must broaden our minds beyond the antics of the nearest zoo chimpanzee.

Still, as the old saying goes, ‘a picture of a crab wearing a sponge or literal shell-suit is worth a thousand words’. To round out this post let’s sit down for a fashion show of the carrying crab world, picking up a few more scientific details along the way, but also taking the time to marvel at what this group of decapods have achieved.

Consider this lot, from a 2015 paper co-authored by Guinot and Wicksten:

Most of the coverings are ascidians—sometimes called sea squirts—which grow attached to the seafloor but are themselves living animals. The crabs need to find one they like, carefully detach it, then either back into it or wriggle around until they can firmly grab hold with those dorsal legs. As you can see, the resulting coverage ranges from almost complete encasement (the Papua New Guinean example in G) to a looser protection (the New Caledonian crab with its sponge, seen from below in A).

There might be another common pattern you’ve noticed in this photo. Have another look, and don’t get distracted by the size or shape of the carried object. Do you see it? As researchers have discovered, the crabs often choose coverings similar in colour to their body. Reddish crabs choose reddish covers, pale crabs pick pale covers, and so on.

Some even enter the hallowed realm of stone tool users, as shown by this Palicoides whitei crab, struggling along with a pebble clasped firmly in its raised fifth legs:

Why go to that kind of trouble? The behaviour must have strong evolutionary purpose to have survived tens of millions of years. And hypotheses abound: is this simply food storage, keeping a healthy snack around for later? The fact that both dead animals and stones are carried, along with the lack of evidence that the crabs eat their shelter, argues against that explanation.

Is it an active deterrent, where the covering is itself toxic or unpleasant to predators? Again, not all coverings are biologically active, although some are—there isn’t enough evidence to suggest that’s the major driver though. By the way, if you’re interested in crab chemical warfare, we’ll be looking at the decorator crabs and their anemone companions another time.

Is it camouflage or concealment then, where the crab either doesn’t get noticed, or a predator fails to learn an association between yummy crab and seemingly walking ascidian? This explanation is currently the most favoured. Recall the matching colour schemes we saw earlier, for one. And it is an idea supported even when the light reaches such low levels that visual concealment would seem to be a non-issue.

Between 2003 and 2010 Andreia Braga-Henriques and her colleagues from the Portuguese Department of Oceanography and Fisheries led a series of dives (in both robotic and crewed submersibles) around the Azores archipelago. At depths of 300-1000m they found crabs of the species Paromola cuvieri happily strolling around carrying soft corals and sponges with their spindly back legs. Again, the ‘edible-covering’ theory was ruled out:

Despite apparently living in lightless conditions, when the research submarine showed up the crabs reacted as you’d expect from a concealment strategy:

All P. cuvieri were moving slowly over the seabed with their walking legs exposed. In close proximity to the submersible ‘LULA’, three of the crabs that were carrying objects stopped moving, lowered the carried object to cover the carapace, thus producing a camouflage effect, and remained still for at least 1 min.

It’s possible that the carrying behaviour is an unnecessary hold-over from the past, when ancestors living higher up in the lit zone would have found it more helpful. But their ‘shelter in place’ reaction to the Portuguese team shows that it’s still at least occasionally useful. We’d need to know a lot more than we do about predator-prey relationships in that part of the deep ocean, as well as the history of the crabs themselves.

In the end, though, perhaps we should draw another lesson with tenuous parallels to human umbrella use: it’s better to have one and not need it, than not have one and get eaten.

Sources: McLay, C. (2020) Rediscovery of the sponge crab Cryptodromia fallax (Latreille in Milbert, 1812) (Decapoda: Brachyura: Dromiidae) at Mauritius, with the description of a new genus and the confirmation of an unusual seaweed-carrying camouflage mode. Journal of Crustacean Biology 40: 82–88. || Wicksten, M. (1986) Carrying behavior in Brachyuran crabs. Journal of Crustacean Biology 6: 364-369. || Guinot, D. & M. Wicksten (2015) Camouflage: carrying behaviour, decoration behaviour, and other modalities of concealment in Brachyura. In Castro, P. et al. (eds) Decapoda: Brachyura (Part 1), Treatise on Zoology – Anatomy, Taxonomy, Biology, vol. 9C-I. Brill, Leiden and Boston. pp. 583–638. || Guinot, D. et al. (2013) Significance of the sexual openings and supplementary structures on the phylogeny of brachyuran crabs (Crustacea, Decapoda, Brachyura), with new nomina for higher-ranked podotreme taxa. Zootaxa 3665 (1): 001–414. || Artal, P. et al. (2008) Ibericancridae, a new dakoticancroid family (Decapoda, Brachyura, Podotremata) from the upper Campanian (Upper Cretaceous) of Spain. Zootaxa 1907: 1–27. || McLay, C. & A. Hosie (2012) Another shell-carrying dromiid crab, Desmodromia tranterae McLay, 2001, from the Dampier Archipelago, Western Australia and observations of shell-acquisition behaviour of Conchoecetes artificiosus (Fabricius, 1798) (Decapoda, Brachyura, Dromiidae). In Komatsu, H. et al. (eds) Studies on Eumalacostraca: a homage to Masatsune Takeda. Brill. pp. 183–196. || Braga-Henriques, A. (2012) Carrying behavior in the deep-sea crab Paromola cuvieri (Northeast Atlantic). Marine Biodiversity 42: 37–46.

Main image credit: McLay (2020) Fig. 3 || Second image credit: McLay (2020) Fig. 4 || Third image credit: McLay & Hosie (2012) Fig. 1 || Fourth image credit: Guinot & Wicksten (2015) Fig. 71-11.3 || Fifth image credit: Guinot et al. (2013) Fig. 54 || Sixth image credit: Braga-Henriques et al. (2012) Fig. 2