The name “hermit” does not rouse images of a complex social life, particularly not one involving the commotion of social aggregations, intergenerational inheritance of homes, and life-or-death competitive struggles. And yet, hermit crabs—terrestrial hermit crabs, in particular—exhibit all this and more. For years I have been studying the social drama playing out underfoot among these small creatures. I have scrutinized the behavior of one species, Coenobita compressus, on the beaches and in the rain forests of Costa Rica where it resides, as well as in the laboratory. We humans are sometimes apt to overlook diminutive invertebrate organisms, letting large, charismatic vertebrates, such as primates and birds, absorb our attention. Yet it is often the tiniest organisms that provide the most exquisite systems for exploring nature and answering fundamental scientific questions. Hermit crabs, despite the “hermit” in their name, have proven quite a useful system for investigating how and why social behavior evolves.
In contrast to many other social organisms, which associate with close kin, terrestrial hermit crabs socialize with nonrelatives. The reason is their dispersal mechanism: the crabs spend their entire adult lives on land, but to reproduce they still need the sea, and into it they release their developing larvae. Once in the ocean, those larvae become well mixed and are transported considerable distances at the whim of the tide. By the time an immature crab first arrives on land, it is therefore far from any of its relatives, encountering instead only an assortment of non-kin. Moreover, because the abundance of terrestrial hermit crabs on short stretches of beach often measures in the hundreds of thousands or even the millions, each crab is but a stranger within a vast crowd. What then is the source of these crabs’ sociality? It’s not the vagaries of the external world— the need to collectively defend against predators, or to come together to eat clumped food resources. No, the sociality of terrestrial hermit crabs is something they have imposed upon themselves due to their own niche construction.
To appreciate the significance of niche construction, consider first that some organisms simply fill a niche, moving into whatever opening or opportunity avails itself, without attempting any modification. Most of the nearly 1,000 species of hermit crabs worldwide are exclusively aquatic, and they accept a given niche as it is. Those hermit crabs occupy the recess of an empty snail shell after the snail has died, and they use the snail’s leftover shell as a portable home, making no alterations to it. In contrast, the approximately dozen species of terrestrial hermit crabs are niche constructors: they actively remodel snail shells, chemically and physically carving out interiors to create an architecture that differs substantially from the snails’ original. Terrestrial hermit crabs thus change their world by constructing remodeled homes. Ultimately, this seemingly trivial architectural act has had stark evolutionary consequences down the line for crabs’ social lives. To make sense of these consequences, though, it is necessary to first ask why terrestrial hermit crabs remodel their shells at all.
Life on land is radically different from life in the sea. And since terrestrial hermit crabs spend most of their lives on land, they experience both pressures and opportunities that are rather unlike those that confront aquatic hermit crabs. Every hermit crab, land or sea, must bear the burden of carrying its home on its back wherever it travels. But for terrestrial hermit crabs this burden is particularly great, because in their environment water buoyancy no longer offers partial support. Instead, the crab itself must entirely support the weight of the shell, which can exceed its own body weight—thus incurring a substantial cost during locomotion. With colleagues in biomechanics, I have experimentally examined those locomotion costs, letting terrestrial hermit crabs walk on a miniature treadmill while measuring their metabolic activity inside an oxygen chamber. Since remodeled shells have a substantially reduced weight compared to unremodeled shells, crabs can decrease their locomotion costs by using remodeled shells. This key selection pressure—lowering travel costs on land—has favored crabs’ niche construction.
At the same time, remodeled shells also afford crabs more internal space, which further enhances their fitness: it offers increased volume for a water reservoir, which can prevent desiccation in the intense tropical sun, and it allows them to grow bigger and store more eggs inside their roomier shell. Aquatic hermit crabs might also conceivably benefit from having a more spacious interior shell. So why is it that they do not remodel their shells and only terrestrial hermit crabs do? Again, the answer stems from differing natural selection pressures on land versus in the sea. The sea contains many predators, such as pufferfishes, stomatopods, and brachyuran or “true” crabs, that have specialized over hundreds of millions of years for removing snails from their shells. Such predators can just as readily target aquatic hermit crabs that secondarily occupy snail shells, so it would be a mistake for an aquatic hermit crab to sacrifice any of the vital protective armature of the shell by remodeling it. In contrast, on land there are few shell-specialist predators, and experiments I have conducted with mechanical engineers—using machines to crush remodeled shells between the jawbones of terrestrial predators— reveal that remodeled shells remain safely outside the bite force of those predators [see bottom image on opposite page]. So even though remodeling weakens shells by removing the architectural support of the shell’s interior spiral axis, a remodeled shell is nevertheless a safe bet for land. Ultimately, therefore, relaxed predation pressures on land enabled terrestrial hermit crabs to benefit from niche construction. Surprisingly, that has social consequences for later generations that fight for remodeled shells.
Evolutionary biologists now increasingly realize that to understand the complex unfolding of the history of life, material inheritance, in addition to genetic inheritance, must be taken into account. The physical modifications that organisms make to their world can generate a kind of ecological inheritance, which may interact with species’ genetic inheritance to shape evolutionary trajectories. An important prediction of niche construction theory is that even small alterations to the world can create an ecological inheritance with profound evolutionary consequences, particularly as it accumulates across generations. Shells are ideal candidates for inheritance (though not in the sense of a family or kin inheritance). Years ago I introduced marked shells into natural populations of terrestrial hermit crabs, and those shells have since lasted across several generations. Interestingly, some populations of terrestrial hermit crabs have even persisted in areas where snails became locally extinct: the crabs utilized a stockpile of fossilized shells from their forebears.
Over time, remodeled shells have come to dominate the housing markets of terrestrial hermit crabs. Exhaustively sampling these housing markets, I have found few unremodeled shells, and also few shells that are still in the process of being remodeled; most shells have already been completely remodeled. Remodeled shells represent a superior home, and as with any superior resource, it is understandable that terrestrial hermit crabs should prefer remodeled shells over unremodeled shells. However, over evolutionary time a mere preference has transformed into an absolute dependence. As remodeled shells accumulated, terrestrial hermit crabs came to specialize in living in them, to the point that life in unremodeled shells became nearly impossible. My field experiments revealed that, after an early life stage, most terrestrial hermit crabs cannot survive in unremodeled shells for even a single day.
One route to acquiring a remodeled shell is to find an empty unremodeled shell and to remodel it yourself from scratch. Unfortunately, this option is physically impossible for most crabs. Remodeling necessitates the crab fit deep inside the shell to access the internal cavity. Only the very smallest—typically still immature—terrestrial hermit crabs can accomplish that feat. Since a crab must continually and fully occupy the shell throughout the remodeling phase, it is paradoxically the smallest crabs that are forced to carry the heaviest shells, for only such big shells have openings large enough for the crab to fit into. The weight of those shells can be too much for their small occupants. To investigate how crabs remodel shells, I have examined the insides of these shells with a scanning
electron microscope, which directs a focused beam of electrons to image fine-grained surface structure. The images suggest that crabs remodel shells by combining chemical secretions—which weaken a shell’s calcium carbonate—with physical sculpting of the shell interior using their appendages. Such actions are
costly, both in time and effort. Indeed, when given the choice between a remodeled shell and an unremodeled shell, all crabs, even those small enough to fit inside an unremodeled shell, opt for an already remodeled shell. Thus, only when the availability of remodeled shells in the housing market becomes sufficiently low will small crabs invest in remodeling. The last resort ensures that remodeled shells do not eventually vanish altogether, but are periodically replenished.
Taking possession of a remodeled shell is highly competitive. In all the populations of terrestrial hermit crabs that I have studied, virtually every remodeled shell has been occupied. Indeed, across miles of beach only a few empty shells can be found, and those typically have some sort of blockage—such as a rock preventing entry—or a gaping hole or breakage. With so few available remodeled shells and with so many crabs eager to move up in the housing market, the demand for remodeled shells clearly outstrips the supply. How, then, should a terrestrial hermit crab go about securing a remodeled shell in such a setting? The answer seems to be: by socializing. For it is only by being highly gregarious and spending time around others that one stands a chance of acquiring a prime shell.
The social lives of terrestrial hermit crabs amount to a near-constant struggle, on the one hand to defend one’s own remodeled shell against theft by others, and on the other hand to strategize about how to take someone else’s remodeled shell. Since shell size is a critical determinant of crabs’ reproductive success, each crab is constantly calculating ways to rise in the housing market by taking the slightly bigger shell of another crab. The prior occupant must either die or be evicted, neither outcome being pretty. (While I have an uncle who is a real estate agent, I sincerely doubt he or others in his profession have ever witnessed anything quite like the disputes of terrestrial hermit crabs.)
Real estate dealings typically begin with one crab climbing onto the back of the shell of another crab. The crab below jostles in response, trying to throw off the one on top. Meanwhile, the top crab gauges the size of the other’s shell and also assesses the other’s relative strength, based on its jostling. If the lower crab gets flipped over, the attacking crab tries to pull it out of its shell. Shell fights, however, are not just two-crab affairs. Other crabs on the sidelines are always alert to a possible eviction, and upon detecting one in progress they flock to the site in large numbers, forming a frenzied crowd as the two antagonists battle it out. My field experiments have revealed that simulated aggregations of several tethered crabs or of several empty shells, jostled to mimic the commotion of evictions, attract terrestrial hermit crabs by the hundreds, and in a matter of minutes. Notably, the same experiments have no effect on species of hermit crabs that are not niche constructors: in the absence of niche construction, such highly social tendencies have not been favored by evolution. Instead, for hermit crabs that fill their niche rather than construct their niche, individuals prefer unremodeled shells and seek shells directly from dying snails, rather than by grappling with fellow hermit crabs.
Ultimately, conflicts among terrestrial hermit crabs over remodeled-shell real estate can be protracted, continuing for hours, sometimes only to end in a stalemate. So why do crabs wait around? They wait because only by being in the right place at the right time might they ever acquire a bigger remodeled shell without incurring the cost of having to evict someone themselves. As bystanders gather at the site and as the moment of eviction nears, order emerges out of the chaos of commotion in the aggregation: the crabs array themselves literally into a line, each holding the shell of the crab ahead of it. This social formation emanates from the pair of antagonists, with the line of crabs thereafter being size-ordered from biggest to smallest. If any crab tries to butt in ahead of another crab that is bigger, then it will be kicked aside and forced to move further back in line. Each crab in the line awaits the decisive moment when the crab at the head of the line is evicted, setting off a vacancy chain, wherein the evictor will move into the evictee’s shell, leaving behind its own shell, and then the next crab in line will rapidly move into the old shell of the evictor, and so on all the way down the line until only the smallest shell of the last crab in line is left. The importance of timing and location cannot be overstated: if a crab is not at the eviction site, ready and waiting in line at the exact moment an eviction occurs, then a split second later the only thing left may be the puniest and most undesirable of empty shells. Sadly, the evicted crab itself is often left naked and in limbo, with the end product of the vacancy chain being a shell that is too small for it to enter. Evicted crabs are therefore liable to die from desiccation or predation, occasionally being lucky enough to find a bottle cap or other substitute as temporary housing.
Observing such ruthless social dynamics play out among terrestrial hermit crabs, one cannot fail to be struck by the stark contrast to an alternative scene, often just a few feet away, involving a far more altruistic invertebrate in the same habitat. Here, lines of cooperating leafcutter ants march back to their nest to feed their colony, each ant in line carrying a large piece of leaf, which, like a hermit crab’s shell, may weigh more than the ant’s own body. The ants, unlike the crabs, are close genetic relatives, and kinship is a key ingredient that favors their cooperation. The lives of these social insects thus represent a sort of antithesis to the lives of “social hermits” like terrestrial hermit crabs: the emphasis is on altruism and cooperation rather than on selfishness and competition. If, in an alternative world, interactions in terrestrial hermit crabs were among close kin rather than strangers, then the crabs’ social lives might be different, with individuals potentially being more interested in bequeathing their finest shell to a close relative than in stealing the coveted shell of a stranger.
One comfort to curious naturalists: biologists have barely scratched the surface in terms of in-depth behavioral study of the nearly 1,000 species of hermit crabs worldwide. Indeed, some species have hardly been examined at all, including deep-sea hermit crabs, whose tighter-knit communities may have greater interaction among their kin, wherein cooperation could trump competition. For those of us who pay attention to the little creatures, therefore, many mysteries still beckon in the social lives of hermit crabs.—M.E.L.