Mark E. Laidre’s research while affiliated with Dartmouth College and other places

Vision is a ubiquitous sensory modality adapted to vastly different environments, which place variable selection pressures on both macro- and microscopic dimensions of external eye morphology. The hermit crab clade (Crustacea: Decapoda: Anomura) spans environments from sea to land, yet, no systematic comparisons in eye morphology have been made between any species. We compared three species of hermit crabs inhabiting different ecological and social environments: two terrestrial species, one of which (Coenobita compressusH. Milne Edwards, 1837) is highly social and inhabits a flat, open diurnal habitat, and another (C. clypeatus Herbst, 1791) is its sister species that inhabits a rugged forested nocturnal habitat; and a third (Pagurus longicarpusSay, 1817) inhabits a marine intertidal habitat and is less social. We compared macroscopic eye morphology between species as well as microscopic differences in ommatidium-facet density and diameter within eyes. We found that eye dimensions (length, width, and thickness), but not overall volume, differed significantly between marine and terrestrial species. Furthermore, the highly social C. compressus had a significantly larger eye volume compared to its sister species, C. clypeatus, which is not as social. Larger eyes in C. compressus might be linked to its social lifestyle, where vision has been shown to be critical to finding conspecifics. All three species had a higher density of facets in the ventral compared to dorsal region of the eye. Our comparisons of external eye morphology revealed microscopic similarities but notable macroscopic variation between species, thus laying a foundation for future phylogenetically controlled tests within this species-rich clade, including comparisons of internal eye morphology.

Conspecifics can provide social cues about the presence of key features of the surrounding environment, such as food or predators. Attending to social cues may therefore potentially benefit receivers, or at least be worth following. Yet, bearing social cues could also be costly, particularly if it increases the likelihood of close-range interaction with non-kin. Here, we experimentally seeded social cues in the wild onto focal individuals of the social hermit crab (Coenobita compressus), testing (1) the “potential benefits to receivers” hypothesis, which predicts that receivers will follow social cues to orient toward valuable resources, and (2) the “costs to bearers” hypothesis, which predicts that bearers of social cues will experience direct (physical) costs or indirect (constrained movement) costs due to interaction with receivers. Consistent with hypothesis (1), in natural encounters, conspecifics that crossed paths frequently made antennal contact, potentially gathering social information at close range. In experiments, naive conspecifics followed focal individuals bearing “positive” social cues (about a valuable food resource) significantly more often than they followed individuals bearing less attractive (“neutral” or “ambivalent”) social cues, pointing to a potential benefit. Consistent with hypothesis (2), individuals bearing positive social cues incurred greater direct and indirect costs, being physically flipped more often and achieving shorter displacements compared to individuals bearing other social cues. We conclude that experimentally seeded social cues in the wild can confer costs to bearers and potentially benefit receivers. Broadly, the costs of bearing social cues, revealed here, underscore the importance of not overlooking that social cues may be costly.

Synopsis Red coloration on a signaler's body may be an informative signal in many animals. For species that inhabit architecture (e.g., burrows, nests, or other structures), certain parts of the body are more exposed than others, potentially serving as superior platforms for signaling via coloration. Yet whether animals differentially advertise red coloration on body parts that are more versus less exposed from their architecture remains to be tested. Here, we systematically quantified red coloration in social hermit crabs (Coenobita compressus). These crabs inhabit architecturally remodeled shells and have claws that visibly block the shell entrance, like doors to their homes. We hypothesized that red coloration of claws may be a signal of resource-holding potential (RHP). Consistent with this RHP signaling hypothesis, we found that within the same individuals’ bodies, exposed claws showed significantly greater red coloration than unexposed carapaces. Furthermore, larger body size predicted greater red coloration of claws. Competing hypotheses (e.g., interspecific signaling, camouflage, and UV protection), while not explicitly tested, nevertheless appear unlikely based on natural history. Red claw coloration may therefore function as a signal to conspecifics, and experiments are now needed to test recipient responses. Broadly, relative to surrounding architecture, exposed body surfaces offer rich potential as signaling platforms for coloration.

Even for animals with multiple senses at their disposal, there may be a strong reliance on a single sense, like vision, for social behavior. Experimentally blocking or eliminating vision offers a powerful means of testing impacts on social behavior, though few studies have followed experimentally blinded individuals in the wild to test potential changes in social behavior in natural settings. Here we conducted experiments with social hermit crabs (Coenobita compressus), applying opaque material overtop their eyes to temporarily blind individuals. We then released these experimentally blinded individuals and non-blinded control individuals into the wild as well as into captive social settings. Compared to control individuals, experimentally blinded individuals initiated significantly fewer social contacts with conspecifics in the wild. These experimentally blinded individuals were not, however, differentially targeted by conspecifics. Interestingly, unlike the wild experiments, the captive experiments showed no differences in social behavior between experimentally blinded and non-blinded control individuals, suggesting that experiments in natural settings in the wild may be essential to fully unraveling impacts of blindness on social behavior. Broadly, for social animals that are highly reliant on the visual modality, social behavior may change dramatically if they lose their vision.

Social organisms form groups with diverse configurations. While the dynamics within social groups have been explored extensively, the perspective of individuals outside of groups has been considered less. Here, we studied social hermit crabs ( Coenobita compressus ) and experimentally tested the perspective of “outsiders”—individuals that were not yet part of a group but were actively searching for a group to join. Using architectural arrays of shells, we simulated a natural social structure—a “social chain”—in which all group members piggyback in sequence. We then tested how outsiders perceived experimentally simulated social chains, which we varied in orientation (horizontal vs. vertical) and which we arranged to be either socially ordered or disordered (i.e., all members arranged in order of size vs. randomly). Outsiders were more attracted to horizontally vs. vertically oriented chains, consistent with a specialization for detecting groups along the horizon. Outsiders were also more attracted to the long rather than the short side of horizontally oriented chains, consistent with the greater perceptual salience of the long side. Finally, outsiders were only marginally capable of determining where they belonged within groups—in terms of size matching—for ordered chains; and they showed no such capability for disordered chains. Broadly, our experiments suggest that a group's configuration, including both its orientation and social ordering, influences outsiders' perceptions and decisions.

Collective movement may emerge if coordinating one’s movement with others produces a greater benefit to oneself than can be achieved alone. Experimentally, the capacity to manoeuvre simulated groups in the wild could enable powerful tests of the impact of collective movement on individual decisions. Yet such experiments are currently lacking due to the inherent difficulty of controlling whole collectives. Here we used a novel technique of experimentally simulating the movement of collectives of social hermit crabs (Coenobita compressus) in the wild. Using large architectural arrays of shells dragged across the beach, we generated synchronous collective movement and systematically varied the simulated collective’s travel direction as well as the context (i.e., danger level). With drone video from above, we then tested whether focal individuals were biased in their movement by the collective. We found that, despite considerable engagement with the collective, individuals’ direction was not significantly biased. Instead, individuals expressed substantial variability across all stimulus directions and contexts. Notably, individuals typically achieved shorter displacements in the presence of the collective versus in the presence of the control stimulus, suggesting an impact of traffic. The absence of a directional bias in individual movement due to the collective suggests that social hermit crabs are individualists, which move with a high level of opportunistic independence, likely thanks to the personal architecture and armour they carry in the form of a protective shell. Future studies can manipulate this level of armour to test its role in autonomy of movement, including the consequences of shell architecture for social decisions. Our novel experimental approach can be used to ask many further questions about how and why collective and individual movement interact.

The evolution of cooperation among non-kin poses a major theoretical puzzle: why should natural selection favor individuals who help unrelated conspecifics at a cost to themselves? The relevance of architecture to this question has rarely been considered. Here I report cooperation among non-kin in social hermit crabs (Coenobita compressus), where unrelated conspecifics work together to evict larger individuals from a housing market of architecturally remodeled shells. I present (1) the first detailed description of natural coalitions in the wild and (2) a theoretical framework, which examines the evolutionary benefits to each coalition member and predicts when forming a coalition will be successful. In the wild, important ecological and social constraints exist, which are built into the model. Based on these constraints, I show that coalitions can be a successful strategy if several key criteria hold: the coalition is necessary, effective, stable dyadically, and stable polyadically. Notably, the “splitting the spoils” problem—which often undermines non-kin cooperation—is eliminated via architecture: a small individual (C) who helps a medium individual (B) to evict a large individual (A) will ultimately benefit, since C will get B’s left behind shell after B moves into A’s shell. Coalitions, however, can break down due to added layers of social complexity involving third-party “free riders” and “cheaters,” which strategically butt in the architectural queue and thereby steal incentives from the smaller coalition member. Overall, therefore, substantial scope exists for both cooperation and conflict within nature’s housing market of architecture. Experiments are now needed to directly test the impact on coalitions of architecture, from the interior of homes up to whole housing markets.

Many animals shape and modify their physical environment, thereby creating a diversity of structures, from underground burrows to constructed nests to towering above-ground edifices, all of which are referred to as ‘animal architecture’. Examples of animal architecture are found everywhere on Earth: beneath the sea and on land, below and above ground, and hanging into the air off trees and precipices. Fossils suggest that animals have been acting as architects by constructing shelters and other built structures for hundreds of millions of years. Animal architects are widespread taxonomically, spanning invertebrates (Figure 1) and vertebrates (Figure 2). Their architectural creations are diverse, including: the fortress-like mounds of termites, the housing markets of architecturally remodeled shells of social hermit crabs, the subterranean tunnel systems of naked mole rats, the intricately decorated bowers of bowerbirds or the engineered dams of beavers. Even the tallest of human architecture is rivaled by animal architecture: termite mounds exceed skyscrapers in their size relative to that of the architects. Animal architecture raises many fascinating questions at the interface of behavior, ecology and evolution: How is this architecture built? What instinctive ‘blueprints’ or cognitive mechanisms underlie its creation? What functions does the architecture serve? And why did it evolve? Notably, because architecture changes the world, it may have far-reaching impacts on collective behavior and social life, interactions among communities of species and whole ecosystems. Architecture may even have altered the very course of evolution.

Architecture, like nests, burrows, and other types of fortresses, may have played an important role in the evolution of social life on land. However, few studies have examined architecture in organisms that transitioned from sea to land to test how and why architectural and morphological changes might have jointly impacted social evolution. Here I contrasted the shell architecture and body morphology of two of the phylogenetically most closely-related land versus sea species of hermit crab (the terrestrial hermit crab, Coenobita compressus, and the marine hermit crab, Calcinus obscurus), as well as the original builder of their shells (the gastropod, Nerita scabricosta). In contrast to the shells of gastropods and marine hermit crabs, only the shells of terrestrial hermit crabs were architecturally remodeled, with no columella inside for the occupants to grip upon to resist eviction. The bodies of terrestrial hermit crabs were also significantly more exposed outside the enlarged openings of their remodeled shells, whereas the substantially smaller-bodied marine hermit crabs were safeguarded deep within the recesses of their unremodeled shells. Ultimately, these changes in shell architecture and body morphology likely had consequences for social evolution on land, making conspecifics not only more dependent upon one another for homes, but also potentially easier to evict. Further changes in claw shape on land (with the claws of terrestrial hermit crabs becoming shorter, wider, and thicker) may have evolved to help offset their heightened danger of social eviction, acting as a more effective door against conspecifics.