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Unlike terrestrial hermit crabs, marine hermit crabs do not prefer shells previously used by conspecifics
Abstract
Gastropod shells represent an essential resource for hermit crabs (Decapoda, Anomura). In many cases, hermit crabs acquire used shells from conspecifics who previously occupied the shell. Terrestrial hermit crabs (Coenobita compressus H. Milne Edwards, 1836) strongly prefer used shells. Here we test whether marine hermit crabs (Pagurus samuelis (Stimpson, 1857)) also exhibit a preference for used shells by providing them with matched pairs of (1) a used shell (previously occupied by either the choosing crab itself or by a conspecific) versus (2) a brand new shell (freshly derived from a predated gastropod). Unlike terrestrial hermit crabs, marine hermit crabs showed no preference for used shells (either their original shell or a shell from a conspecific). We suggest the divergent shell preferences of marine and terrestrial hermit crabs relate to the contrasting natural selection pressures in the sea versus on land. In particular, the used shells of terrestrial hermit crabs are architecturally remodeled by prior occupants and these remodeled shells represent a superior resource on land. In contrast, marine hermit crabs never remodel shells, and for them a used shell may be less protective than a new shell against the many specialized shell predators in the ocean.
... To rigorously evaluate the extent to which substrate-borne vibrations actually function to resolve conflicts, it is essential for studies to experimentally simulate different levels of these vibrations, independent of other modalities [1][2][3], to test whether it is the vibrations themselves that generate differential responses. One system that lends itself to such a test is the highly social terrestrial hermit crab (Coenobita compressus) [9], which, unlike other hermit crab species [10], is entirely reliant upon conspecifics [11] as a source of their most valued resource, architecturally remodelled shell homes [12]. Social competitors in this species frequently 'piggyback' on the dorsal side of a conspecific's home, assessing the exterior while the homeowner remains fully retracted inside [13]. ...
... And finally, when the owner was 'extremely weak' (too weak to vibrate) or 'entirely absent' (no vibration), crabs showed the longest assessment times and the highest likelihood of conflict escalation. Given that architecturally remodelled homes are valuable in this highly social species [9][10][11][12][13], and that remodelled homes lacking an owner are virtually non-existent [16,17], the differential responses shown here to vibration suggest that individuals can gauge owners' strength using vibrations alone. Indeed, regardless of whether vibrations are a byproduct 'cue', incidentally correlating with RHP [5], or are a 'signal' that evolved specifically to advertise RHP [2,3], these vibrations seem to offer an index of the owner's ability to defend its home, thereby helping to resolve property conflicts. ...
Animals may use a variety of sensory modalities to assess ownership and resource-holding potential (RHP). However, few studies have experimentally tested whether animals can assess these key variables through a purely vibrational modality, exclusively involving substrate-borne vibrations. Here we studied social terrestrial hermit crabs (Coenobita compres-sus), where competitors assess homeowners by climbing on top of a solid external structure-an architecturally remodelled shell home, inside of which the owner then produces vibrations. In the field, we used a miniature vibratory device, hidden within an empty shell, to experimentally simulate a 'phantom owner', with variable amplitudes of vibration representing different levels of homeowner strength. We found that assessors could use these vibrations to deduce the owner's RHP: for strong vibrations (indicative of a high RHP owner) assessors were least likely to escalate the conflict; for weak vibrations (indicative of a low RHP owner) assessors showed intermediate escalation; and in the absence of vibration (indicative of an extremely weak or absent owner) assessors were most likely to escalate. These results reveal that animals can assess homeowner strength based solely on substrate vibrations, thereby making important decisions about whether to escalate social conflicts over property.
... The risk of property theft during sex is differentially high in some species of hermit crab, which architecturally modify shells [13 -16], rendering these shells more valuable and more easily stolen private property [12,17,18]. Specifically, unlike marine hermit crabs [19], terrestrial hermit crabs (Coenobita spp.) remodel the interior of shells and these costly construction efforts [20] make remodelled shells highly preferred and more valuable resources. Indeed, while resource value differences exist in marine hermit crabs (which prefer certain shell species over others), the magnitude of such differences is dwarfed by the difference in resource value between remodelled versus unremodelled shells in terrestrial hermit crabs: without a remodelled shell, adult terrestrial hermit crabs will desiccate and die within 24 h, even if given an unremodelled shell in exchange [17]. ...
... For species with more valuable and more easily stolen property, a longer penis can thus extend out of a male's shell and into a female's shell, allowing both parties to maintain more secure, decisive grips on their property by not coming out as far of their shells. The evolutionary pattern of relative penis size across species is consistent with this 'private parts for private property' hypothesis, especially the intense level of social competition for remodelled shells that exists within the housing markets of Coenobita species [9][10][11][12][13][14][15][16][17][18][19][20]22]. Critically, all other hypotheses for these penis size patterns came up short. ...
Evolution has generated enormous diversity in animal genitalia. However, the importance of private property in driving penis size evolution has rarely been explored. Here, I introduce a novel hypothesis, the ‘private parts for private property' hypothesis, which posits that enlarged penises evolved to prevent the theft of property during sex. I tested this hypothesis in hermit crabs, which carry valuable portable property (a shell) and which must emerge from this shell during sex, risking social theft of their property by eavesdroppers. I measured relative penis size (penis-to-body ratio) for N = 328 specimens spanning nine closely related species. Species carrying more valuable, more easily stolen property had significantly larger penis size than species carrying less valuable, less easily stolen property, which, in turn, had larger penis size than species carrying no property at all. These patterns in penis size remained even when phylogeny was controlled for, and the patterns were not explained by alternative hypotheses. Instead, the results suggest larger penises evolved as morphological adaptations to facilitate safe sex, in which individuals retain their valuable property by extending a long penis outside the shell to copulate. This hypothesis may likewise apply to other taxa, including those with valuable but non-portable property.
... While in theory conspecifics that already occupy shells could provide a rich source of these resources, only terrestrial hermit crabs are uniquely dependent upon socially-derived shells (Laidre 2012a(Laidre , 2014. Marine hermit crabs, in contrast, specialize on and prefer brand new shells, deriving directly from living gastropods and never before having been occupied by a conspecific (Laidre and Trinh 2014). Critically, in marine environments, gastropods are preyed upon by a variety of predators (Alcaraz and Arce 2017) and, paradoxically, some of this predation may create new resources. ...
... With many individuals independently orienting to sites of non-destructive shell predation, some may overlap and be forced to compete for the same shell. Indeed, given that marine hermit crabs prefer brand new shells acquired directly from predators rather than used shells previously occupied by conspecifics (Laidre and Trinh 2014), strong pressures exist to arrive at predation sites before others. Individuals that are more sensitive to lower concentrations of the relevant chemical cues or that respond faster will have the best chance of 'beating the crowd' and being first to acquire a new predator-generated shell. ...
Complex environments present substantial spatio-temporal uncertainty in where and when rare ecological resources become available. How animals navigate this uncertainty to turn the seemingly unpredictable into the predictable is a fundamental question in evolutionary ecology. Here we use subtidal hermit crabs (Pagurus acadianus) as a model system to experimentally test in the field how animals resolve spatio-temporal uncertainty in resource availability. Quadrat sampling within the subtidal zone revealed that hermit crabs face an extreme ecological challenge, based on the rarity of empty shells across space and time. We show how this spatio-temporal uncertainty is ultimately resolved using long-distance chemical cues, which are associated with non-destructive shell predation on living gastropods, the original source of shells. By experimentally releasing cues that simulated the chemical by-products of predation, we reveal that certain flesh cues provide fine-grained information about the precise spatial and temporal window of new shell availability. These cues were most attractive to individuals with the greatest existing resource needs, and in the absence of this information individuals were highly constrained in their ability to discover newly available resources. Broadly, these experiments reveal that exploiting simple cues from heterospecific predators can provide a solution to the general ecological challenge of finding resources that are rare in space and time.
... The presence of highly specific, shell-related cues (released by predatory gastropods during the consumption of smaller, shell-inhabiting prey) is thought to be critical in attracting hermit crabs to these shell-acquisition sites (Rittschof 1980b). Indeed, shells freshly-derived from predated gastropods may be more desirable to marine hermit crabs than shells previously used by conspecifics (Laidre and Trinh 2014). ...
... study was carried out between November 2011 and April 2012 at the Bodega Marine Laboratory, located on the Bodega Marine Reserve in Sonoma County, Northern California. The laboratory occupies a pristine rocky intertidal area, which has been the focus of prior field (Laidre and Greggor 2015) and laboratory (Laidre and Trinh 2014) experiments on marine hermit crabs. ...
Competition for limiting resources drives animal aggression. Aggression in hermit crabs has been well studied in shell acquisition contexts, yet less is known about hermit crabs’ competitive behavior in other contexts, especially feeding contexts. As active foragers, competition for food resources may be a major determinant of hermit crab aggression and fighting behavior, particularly in intertidal marine environments in which protein-rich carrion may be limiting. Here we measured aggressive, competitive interactions between hermit crabs (Pagurus samuelis) (Stimpson, 1857) that were presented with carrion in the laboratory, immediately after they were collected from the field. Aggregations of three crabs were provided with either mussel or gastropod flesh. Both forms of carrion naturally indicate food availability, though only the latter may correlate with potential shell availability. We found that levels of aggression rose significantly in response to both carrion conditions, but not in response to a control condition involving the introduction of a non-eatable object. Larger individuals displayed the highest levels of aggressive behavior, but levels of aggression did not differ between the gastropod versus the mussel. These results reveal that food—independent of a shell resource—can be a powerful motivator for competitive behavior in hermit crabs. Further studies of food-related aggression between different hermit crab species could shed light on how interspecific competition might lead to potential specializations on different carrion or prey resources.
... The presence of highly specific, shell-related cues (released by predatory gastropods during the consumption of smaller, shell-inhabiting prey) is thought to be critical in attracting hermit crabs to these shell-acquisition sites (Rittschof 1980b). Indeed, shells freshly-derived from predated gastropods may be more desirable to marine hermit crabs than shells previously used by conspecifics (Laidre and Trinh 2014). ...
... study was carried out between November 2011 and April 2012 at the Bodega Marine Laboratory, located on the Bodega Marine Reserve in Sonoma County, Northern California. The laboratory occupies a pristine rocky intertidal area, which has been the focus of prior field (Laidre and Greggor 2015) and laboratory (Laidre and Trinh 2014) experiments on marine hermit crabs. ...
Competition for limiting resources drives animal aggression. Aggression in hermit crabs has been well studied in shell acquisition circumstances, yet less is known about hermit crabs' competitive behavior in other contexts, especially as they relate to feeding. As active foragers, competition for food resources may be a major determinant of hermit crab aggression and fighting behavior, particularly in intertidal marine environments, where protein-rich carrion may be limiting. Here, we measured aggressive, competitive interactions between hermit crabs [Pagurus samuelis (Stimpson, 1857)] that were presented with carrion in the laboratory, immediately after they were collected from the field. Aggregations of three crabs were provided with either mussel or gastropod flesh. Both forms of carrion naturally indicate food availability, though only the latter may correlate with potential shell availability. We found that levels of aggression rose significantly in response to both carrion conditions, but not in response to a control condition involving the introduction of a non-eatable object. Larger individuals displayed the highest levels of aggressive behavior, but levels of aggression did not differ between crabs provided with the gastropod and the mussel flesh. These results reveal that food-independent of a shell resource-can be a powerful motivator for competitive behavior in hermit crabs. Further studies of food-related aggression between different hermit crab species could shed light on how interspecific competition might lead to potential specializations on different carrion or prey resources. © 2016 Rosenstiel School of Marine and Atmospheric Science of the University of Miami.
... For example, an individual on stair C cannot leap directly up to stair A, without first moving to stair B (Figure 3). This architectural constraint exists because too large a shell-relative to an individual's current body size-is suboptimal (Laidre and Trinh, 2014). Indeed, for a small bodied individual to carry the weight of too large a shell, is energetically costly and inhibits its growth (Osorno et al., 2005). ...
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.
... For now, let us treat this part of the analysis as a "black box" with an unknown and merely roughly estimated quantity of added degrees of freedom. 22 The crabs greatly prefer previously modified over previously unmodified shells (Laidre 2019, Laidre & Trinh 2014. 23 On the range and average number of crabs in these gatherings, see Laidre 2019. ...
There are at least two senses in which human beings can be called “naturally artificial”: (1) being adapted for creation of and participation in niche constructed environments, and (2) being adapted for creation of and participation in such environments despite an exceptional indeterminacy in the details of the niche constructed environments themselves. The former puts human beings in a common category with many niche-constructing organisms while the latter is arguably distinctive of our species. I explain how this can be so by developing an account of supporting concepts of complexity, contingency, and content-openness, and show how to defend the position against a common style of objection by a single comparative case study: hermit crabs and their shells versus humans and their movable dwellings. Finally, I consider evidence that such a feature is indeed species-typical and evolved in human populations.
... This is particularly true in the crustacean world, where our best understanding of the scope of fighting behaviors and the use of weapons and defenses comes from readily observable Stomatopod contest, weapon, and defense 9 near-shore groups of decapods (e.g., fiddler crabs: Dennenmoser and Christy 2013;Swanson et al. 2013;hermit crabs: Briffa et al. 1998;Lane and Briffa 2020). Crustaceans in terrestrial and aquatic environments encounter different physical challenges and selection pressures that could affect the biomechanical traits of their weapons and defenses, as well as the fighting behaviors (Laidre 2014;Laidre and Trinh 2014). With the exceptional diversity of decapods and their presence in habitats spanning the deep sea to tree canopies, this group presents a rich, barely tapped system that is ripe for new discoveries and insights into the evolution of weapons, defenses, and agonistic behavior. ...
In the spirit of this symposium on the physical mechanisms of behavior, we review mantis shrimp ritualized fighting, from the telson to the attack, as an inspiring example of how the integration of biomechanics and behavioral research can yield a penetrating narrative for how animals accomplish important activities, including agonistic actions. Resolving conflicts with conspecifics over valuable resources is an essential task for animals, and this takes an unusual form in mantis shrimp due to their powerful raptorial appendages. Decades of field and laboratory research have provided key insights into the natural agonistic interactions of diverse mantis shrimp species, including how they use their raptorial weapons against one another in telson sparring matches over cavities. These insights provided the foundation for functional morphologists, biomechanists, and engineers to work through different levels of organization: from the kinematics of how the appendages move, to the elastic mechanisms that power the strike, and down to the structure, composition, and material properties that transmit and protect against high-impact forces. Completing this narrative are studies on the defensive telson and how this structure is biomechanically matched to the weapon and the role it plays in ritualized fighting. The biomechanical understanding of the weapon and defense in mantis shrimp has, in turn, enabled a better understanding of whether mantis shrimp assess one another during contests and encouraged questions of evolutionary drivers on both the arsenal and behavior. Altogether, the body of research focused on mantis shrimp has presented perhaps the most comprehensive understanding of fighting, weapons, and defenses among crustaceans, from morphology and biomechanics to behavior and evolution. While this multi-level analysis of ritualized fighting in mantis shrimp is comprehensive, we implore the need to include additional levels of analysis to obtain a truly holistic understanding of this and other crustacean agonistic interactions. Specifically, both molting and environmental conditions are often missing from the narrative, yet they greatly affect crustacean weapons, defenses, and behavior. Applying this approach more broadly would generate a similarly profound understanding of how crustaceans carry out a variety of important tasks in diverse habitats.
... These results strongly suggest that hermit crabs themselves are not responsible for the differences in composition between shell availability and utilization that might arise through acquisition of empty shells by killing their living occupants. Laidre (2012b) and Laidre & Trinh (2014) showed that terrestrial hermit crabs have a greater preference for shells with a larger capacity and lighter weight, which have been remodeled by resident individuals, than the original shells. In the present shellselection experiment, the internal capacity of the empty shells was not dependent on shell selection by marine hermit crabs, as the capacity did not differ between O. rusticus and C. turbinatum. ...
The relative proportions of gastropod shells occupied by the hermit crabs Pagurus dubius (Ortmann, 1892), P. filholi (De Man, 1887), P. lanuginose De Haan, 1849, and P. nigrofascia Komai, 1996 on a boulder shore at Asamushi, northern Japan differ significantly from those of the living gastropods that leave behind their empty shells after death. There is a difference in the frequencies of the shells of Omphalius rusticus (Gmelin, 1791) and Chlorostoma turbinatum A. Adams, 1853, which resemble each other in shape, between the proportions of shells occupied by the living gastropods and those of their empty shells occupied by hermit crabs. The three species of hermit crabs that were dominant at the study site showed no difference in shell selectivity between the two gastropod species in the laboratory. This result indicates that shell selection by hermit crabs cannot be responsible for the difference in composition between availability and utilization observed in the field. The empty shells of O. rusticus are thicker and heavier than those of C. turbinatum, suggesting that the former last longer than the latter, as shell durability against compressive force decreases as shell thickness is reduced. These observations suggest that the difference in the period for which these empty gastropod shells remain intact accounts for the difference in composition between their availability and utilization by hermit crabs.
... For terrestrial hermit crabs, therefore, individuals must specifically interact socially with conspecifics if they are to capitalise on opportunities for remodelled shells (Laidre, 2018b). In contrast, while marine hermit crabs do engage in fights with conspecifics for unremodelled shells (Briffa et al., 1998;Elwood & Briffa, 2001;Briffa & Elwood, 2004;Briffa, 2006;Briffa & Williams, 2006;Arnott & Elwood, 2007;Briffa & Dallaway, 2007;Briffa & Fortescue, 2017), marine hermit crabs can acquire unremodelled shells in the wild directly from predated snails (McLean, 1974;Rittschof, 1980;Wilber & Herrnkind, 1984;McGuire & Williams, 2010;Laidre, 2011;Laidre & Trinh, 2014;Valdes & Laidre, 2018), which substantially reduces marine hermit crabs' need to interact with conspecifics (Valdes & Laidre, 2019). ...
Fitness can be increased dramatically by communication. So why, given the benefits of communication, would displays ever be completely lost evolutionarily? Threat displays, in particular, are relatively cheap to produce and are precursors of attack, so should be especially hard for both senders and receivers to lose completely. Here we explore an evolutionary transition in sociality, testing whether complete evolutionary loss of threat display has occurred in ‘more social’ hermit crab species, which interact more frequently with conspecifics. First, we synthesised literature and observations on the presence versus absence of threat display across hermit crab species, mapping this information onto a phylogenetic tree. We found that all ‘less social’ species — marine and terrestrial — produce threat displays, consistent with threat display being the ancestral state. But ‘more social’ terrestrial species, which are highly derived, do not produce a threat display, suggesting an evolutionary loss. Next, we contrasted natural interactions in the wild within a less social species (Pagurus bernhardus) versus within a more social species (Coenobita compressus), finding that the less social species, despite a lower rate of social encounter, had a higher rate of display per encounter (24%). In contrast, the more social species’ rate of display per encounter was negligible (<1%), effectively indicating a loss in production. Finally, we experimentally reanimated threat display in the more social species, using postured models to test whether receivers retained any responsiveness to threat display. Starkly, receivers were not deterred by threat display, showing equal responsiveness across both threat and non-threat models, regardless of whether the models were stationary or dynamically moving. Our results thus reveal a case of complete collapse of communication involving threat display, implicating the social environment in this loss. In more social species, an extreme dependence on conspecific-derived shells likely drove a ‘desperado effect’, with threat displays being lost because they could not stop others from pursuing these valuable resources.
... Hermit crabs naturally select diverse varieties of vacant molluscan shells, particularly gastropod shells,which makes shell a major limiting resource for their survival (Ohmori et al., 1995;Barnes, 1999;Mantelatto and Garcia, 2000;Meireles et al., 2008;Laidre and Trinh, 2014). Shell utilization process by hermit crabs are determined by shell dimensions. ...
Extensively distributed along tropics and subtropics, terrestrial hermit crabs play critical roles in coastal ecology and they often show preferences towards few gastropod shells in natural ecosystems. The nature of selection of empty gastropod shells as protective 'home' from natural environment for shelter varies with species. In this study the vacant shell search and selection by the terrestrial hermit crab Coenobita rugosus (Coenobitidae; Crustacea) was found to be governed by various parameters including the presence of vacant shells in vicinity, types of vacant shells, and morphometric characters of shells. Laboratory simulation for 72 hours of exposure of hermit crab to different types of vacant host shell combinations followed by statistical evaluation revealed specific relationship in shell selection by hermit crab with morphometric characteristics of vacanthost shells.They also exhibit a greater plasticity in shell selection.
... Critically, these terrestrial hermit crabs face different selective pressures than marine hermit crabs in acquiring shells following death. Marine hermit crabs are specialized to live in unremodeled shells, which can derive either from the death of a gastropod or of any marine hermit crab (Laidre & Trinh, 2014), making both heterospecific and conspecific death equally significant for these marine species. In contrast, such unremodeled shells are effectively unusable by terrestrial hermit crabs (Laidre, 2012a). ...
All living organisms must eventually die, though in some cases their death can bring life‐giving opportunities. Few studies, however, have experimentally tested how animals capitalize on conspecific death and why this specialization would evolve. Here, we conducted experiments on the phylogenetically most closely‐related marine and terrestrial hermit crabs to investigate the evolution of responses to death during the sea‐to‐land transition. In the sea, death of both conspecifics and heterospecifics generates unremodeled shells needed by marine hermit crabs. In contrast, on land, terrestrial hermit crabs are specialized to live in architecturally remodeled shells, and the sole opportunity to acquire these essential resources is conspecific death. We experimentally tested these different species’ responsiveness to the scent of conspecific versus heterospecific death, predicting that conspecific death would have special attractive value for the terrestrial species. We found the terrestrial species was overwhelmingly attracted to conspecific death, rapidly approaching and forming social groupings around conspecific death sites that dwarfed those around heterospecific death sites. This differential responsiveness to conspecific versus heterospecific death was absent in marine species. Our results thus reveal that on land a reliance on resources associated exclusively with conspecifics has favored the evolution of an extreme collective attraction to conspecific death.
... Furthermore, these crabs perform architectural remodelling of their shells, making the inner part thinner, thereby decreasing the mass but also its resistance to being crushed by predators ). Contrary to the terrestrial environments and other sites with low predation, in which relatively small shells with thin walls provide suffi cient protection to hermit crabs, the use of these shells in tropical tide pools with high predatory pressure makes them highly vulnerable to shell-breaking predators (Bertness andCunningham 1981, Laidre andTrinh 2014). ...
Prey exposed to predators with different hunting and feeding modes are under different selective pressures, therefore it is expected that they should exhibit plastic and adaptive antipredator responses according to current risks. The hermit crab Calcinus californiensis faces two contrasting predators, the shell peeler Arenaeus mexicanus that hunts by active searching and the shell breaker Eriphia squamata that hunts by ambush. In order to discover whether C. californiensis displays plastic responses depending on the type of predatory challenge, we examined the shell size preference, the hiding time, and the escape velocity of hermit crabs in the presence of chemical cues from a shell peeler, a shell breaker, and a control. We also examined the role of shell fit on the escape velocity of the hermit crabs in natural tidal pools. Crabs chose shells with a loose fit (relatively large shells) in the presence of chemical cues from the shell peeler Arenaeus and shells with a tight fit when exposed to cues from the shell breaker Eriphia. The hermit crabs hid for shorter times and moved away faster from Eriphia than from Arenaeus stimulus. The use of a tight shell favours faster movement away from the shell breaker (pre-capture strategy), but prevents the crab retracting deeper inside the shell, increasing the risk of be eaten by the shell peeler once captured. Hence, the use of loose shells that protect the crab from the shell peeler hinders fast escape. This study shows specific and plastic antipredatory responses to contrasting predators, each bringing adaptive benefits at different levels of the predator sequence. This article is protected by copyright. All rights reserved.
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.
Animals have been specialized by natural selection to perceive features of their environment that strongly impact their reproductive success. For many social animals, the social world of conspecifics provides the most pertinent information, ultimately enabling individuals to adaptively anticipate future events, like time-sensitive opportunities to acquire rare resources. Here we investigated whether ‘social timing’—joining others at the right time for resource acquisition—ultimately drives the perception of different social structures among highly social terrestrial hermit crabs, Coenobita compressus. These crabs are specialized to live in architecturally remodelled homes, which can only be acquired through coordinated social interactions among conspecifics. We experimentally simulated these social interactions using static arrays of shells that mimicked the temporary social structures formed at each stage in the social shell-acquisition process. Free-wandering crabs in the wild were then allowed to choose among these different social structures. We found that crabs were most attracted to social structures representing early stages of the social shell-acquisition process, which predict forthcoming opportunities and hence allow individuals to join in time to take priority spots in ensuing social formations. In contrast, social structures representing late stages of the social shell-acquisition process were less attractive. When crabs joined such late-stage social structures they did not stay long, assessing they had arrived too late to insert themselves into the existing social arrangement. Broadly, these results suggest that strong selective pressures exist for sensory specializations that are in tune with the temporal and spatial patterning of opportunities in the social world.
Animals’ cognitive abilities can be tested by allowing them to choose between alternatives, with only one alternative offering the correct solution to a novel problem. Hermit crabs are evolutionarily specialized to navigate while carrying a shell, with alternative shells representing different forms of ‘extended architecture’, which effectively change the extent of physical space an individual occupies in the world. It is unknown whether individuals can choose such architecture to solve novel navigational problems. Here, we designed an experiment in which social hermit crabs (Coenobita compressus) had to choose between two alternative shells to solve a novel problem: escaping solitary confinement. Using X-ray microtomography and 3D-printing, we copied preferred shell types and then made artificial alterations to their inner or outer shell architecture, designing only some shells to have the correct architectural fit for escaping the opening of an isolated crab’s enclosure. In our ‘escape artist’ experimental design, crabs had to choose an otherwise less preferred shell, since only this shell had the right external architecture to allow the crab to free itself from isolation. Across multiple experiments, crabs were willing to forgo preferred shells and choose less preferred shells that enabled them to escape, suggesting these animals can solve novel navigational problems with extended architecture. Yet, it remains unclear if individuals solved this problem through trial-and-error or were aware of the deeper connection between escape and exterior shell architecture. Our experiments offer a foundation for further explorations of physical, social, and spatial cognition within the context of extended architecture.
Organisms architecturally modify environments and these modifications may persist across generations, potentially strongly shaping social behavior. However, few experiments have directly tested the impact of architectural modifications from earlier generations on social behavior in later generations. Here I report experiments using extremely durable resources, shells, which endure for decades to centuries in stable form. Terrestrial hermit crabs (Coenobita compressus) architecturally remodel shells and pass these modified shelters to subsequent generations, which reuse them long after the original architect's death. I conducted controlled field experiments in a population of these crabs in which shells have been individually marked and tracked for a decade. I examined the impact of architectural modifications by contrasting social behavior around introduced shells, either remodeled shells (whose internal architecture was modified by earlier generations) or unremodeled shells (whose architecture had never been modified). Remodeled shells generated radically different social dynamics than unremodeled shells, catalyzing vacancy chains in which shells were socially redistributed across the population. Social groups that formed around remodeled shells consisted of size‐ordered queues, with precise timing and social coordination required if individuals were to acquire superior shells. Interestingly, comparative experiments in two non‐architect species (Clibanarius albidigitus and Calcinus obscurus) failed to show any impact of architectural modifications on social behavior; such impacts were only found in the architect species (Coenobita compressus). Broadly, architecture from earlier generations can thus play a major role in driving social dynamics among later generations. This article is protected by copyright. All rights reserved.
Cuantificar la variación de la biodiversidad es un objetivo importante
de la biología. Sin embargo, debido a que tales inventarios, en especial
para la biodiversidad marina, son costosos, difíciles y consumen
mucho tiempo, hay un gran valor en indicadores simples que permitan
determinar la biodiversidad de una región determinada de manera
eficiente. Hicimos un inventario de las conchas usadas como casas
móviles terrestres por los cangrejos ermitaños (Coenobita compressus)
en la Península de Osa, Costa Rica, un “punto álgido” de biodiversidad.
Se registraron 41 especies, el mayor número registrado en cualquier
población de cangrejos ermitaños. Proponemos que la “diversidad del
mercado de vivienda” en los cangrejos ermitaños puede proporcionar
un índice de biodiversidad ecosistémica conveniente, lo que podría
facilitar las comparaciones entre sitios.
ABSTRACT
Quantifying variation in biodiversity is an important goal of biology.
However, because inventorying biodiversity, especially marine
biodiversity, is costly, difficult, and time consuming, there is great value
in simple metrics that can reliably indicate a given region’s biodiversity
and that can be efficiently gathered. We inventoried shells used as
portable houses by terrestrial hermit crabs (Coenobita compressus) in
Osa Peninsula, Costa Rica, a biodiversity hotspot. Forty-one species were
recorded, the largest number registered for any hermit crab population.
We propose that housing market diversity in hermit crabs might provide
a convenient biodiversity index of ecosystems, potentially facilitating
comparisons across different sites.
Greenaway, P. 2003. Terrestrial adaptations in the Anomura (Crustacea: Decapoda). In: Lemaitre, R., and Tudge, C.C. (eds), Biology of the Anomura. Proceedings of a symposium at the Fifth International Crustacean Congress, Melbourne, Australia, 9-13 July 2001. Memoirs of Museum Victoria 60(1): 13-26. In this review, morphological, physiological and behavioural adaptations to life on land by anomurans are considered. The most terrestrial group are the Coenobitidae and these have developed terrestrial adaptations broadly similar to those of the terrestrial brachyurans. The coenobitids have developed two evolutionary, terrestrial lines. Coenobita spp. retain the protective gastropod shell and this has placed a set of constraints on morphological, physiological and behavioural development particularly in regard to gas exchange, osmoregulation and excretion. Birgus do not carry molluscan shells after the juvenile stages and, freed from its constraints, reach larger size and have developed terrestrial adaptations that closely parallel those of the brachyuran land crabs. Shell retention by Coenobita has resulted in development of novel abdominal gas exchange organs whilst purine excretion by B. latro seems to be unique amongst land crabs. Crabs of both genera are well adapted to life on land in terms of sensory, respiratory, excretory and osmoregulatory functions and they can also moult, mate and lay eggs effectively on land. Several species have the functional ability to live in a range of habitats from rainforest to arid scrubland but their penetration of these habitats is limited to small islands or to a narrow coastal strip. This is probably due to the retention of pelagic larval stages and to the lack of molluscan shells of suitable dimensions and strength in inland situations, which restrict the range to a manageable distance from the sea.
Architectural creations occur throughout the animal kingdom, with invertebrates and vertebrates building structures such as homes to maximize their Darwinian fitness. Animal architects face many trade-offs in building optimally designed structures. But what about animals that do not build, and those that only remodel the original creations of others: do such secondary architects face similar trade-offs? Recent evidence has revealed that hermit crabs-animals well known for opportunistically moving into remnant gastropod shells-can also act as secondary architects, remodelling the shells they inherit from gastropods. Remodelling has only been found among terrestrial hermits (Coenobita spp.), not marine hermits. Here we investigate the potential trade-offs Coenobita compressus faces from remodelling by subjecting its remodelled and unremodelled homes to controlled engineering crush tests, which parallel the homes being crushed by predators. While remodelled homes are significantly more spacious and lightweight than unremodelled homes, we find that the homes attain these beneficial qualities at a cost: a reduced resistance to being crushed. Hermit crabs may therefore only remodel their homes to thresholds set by the bite force of their predators. Our results suggest that, like primary animal architects, which face trade-offs when optimizing architectural designs, secondary animal architects face trade-offs when remodelling such designs.
The hermit crab Pagurus longicarpus was shown to inhabit shells that were partially predated from intertidal areas of Long Island, New York. Among field collections
of P. longicarpus, 2.13% of the hermit crabs (46 of 2155) were found with shells with snail tissue present. Over 90% of these partially predated
snail shells were occupied by male hermit crabs. Although hermit crabs were in 8 species of snail shells, only Littorina littorea and Nassarius obsoletus were found occupied by hermit crabs and containing snail tissue. In the laboratory, we found that specimens of the spider
crab Libinia emarginata were able to pull off the operculum of snails, leaving damage as found in field collections. In contrast, specimens of P. longicarpus were not able to prey on live, healthy snails. When specimens of P. longicarpus were placed in communal tanks, hermit crabs preferred partially predated snail shells to empty and original shells. However,
original shells and empty shells were occupied with more frequency than partially predated shells when crabs were isolated.
These findings indicate P. longicarpus actively seeks shells soon after attack and abandonment by snail predators, especially in the presence of competitors.
Animals from invertebrates to humans benefit from information conspecifics make available, including information produced inadvertently. While inadvertent social information may frequently be exploited in nature, experiments have rarely been conducted in the wild to examine how such information helps animals in their natural ecology. Here I report a series of field experiments on free-living terrestrial hermit crabs (Coenobita compressus), showing how these asocial invertebrates learn the locations of their most essential resources, food and shelter, using inadvertent cues from conspecific competitors. Crabs have limited abilities to locate resources individually, but as they coalesce on a resource, their aggregation can be noticed by passing foragers, tipping them off about the discovery. Foragers were strongly attracted to experimentally simulated aggregations in which crabs were tethered to the same spot and in which the resources normally found beneath aggregations were excluded. Simulated aggregations of crabs whose shells were removed were likewise attractive, more than even these sought-after-shelters themselves. Experiments that simulated the chemical and visual cues of aggregations independently revealed that foragers oriented to aggregations primarily by sight, cueing in on the jostling competitive activity of the aggregation. Although crabs have not been selected to recruit others to newly discovered resources, their natural ecology has provided a setting where competitors regularly help one another by means of inadvertent social information.
Understanding the process by which limiting resources are incorporated into populations is a major goal of ecology. While many studies have examined this dynamic process using essential resources like homes, few of these studies have involved homes that can be transported by their occupants. This study introduced over a thousand transportable homes into a population of terrestrial hermit crabs Coenobita compressus, animals that carry their homes with them wherever they travel. These new homes were tracked between years to test key predictions about the temporal dynamics the homes would generate, and the spatial and structural changes the homes would undergo as they were used by the population. When moving into new homes, crabs dropped off their old homes directly at the exchange site, and the number of such traded‐in homes peaked rapidly in time. Traded‐in homes were under half the diameter of new homes, a difference apparently magnified by social formations involving vacancy chains. After crabs moved into new homes, they carried the homes away from the exchange site. The following year, these homes were displaced a distance four orders of magnitude times their diameter, thus penetrating extensively through the population. Between years, crabs also remodeled the internal architecture of the homes, creating homes that were more spacious and less of a burden to carry. These results suggest that transportable homes generate novel ecological dynamics along temporal, spatial and structural dimensions, which are a direct consequence of their transportability.
The herbivorous gastropod Tegula funebralis is not highly ranked in a food preference hierarchy of its major predator, the starfish Pisaster ochraceus, and exhibits a persistent broad overlap with it in the rocky intertidal zone at Mukkaw Bay, Washington. Observations on Tegula over a 5-yr period indicate that it settles high intertidally, lives there for 5-6 yr, and then tends to migrate lower into contact with Pisaster. Tegula lays down an annual growth line permitting it to be aged and a growth curve constructed. Analysis of relative growth and reproduction indicates that beyond a certain size (16 mm) large individuals perform less well in the upper than those in the lower intertidal zone. Pisaster consumes 25-28% of the adult Tegula per year in the area of spatial overlap, based on analysis of the age structure of 6-17 yr old Tegula, and by direct estimates of the percentage of the standing crop consumed annually. The relationship between Pisaster and sex ratio, relative energy limitation and reproductive output (fitness) of Tegula is discussed for three subpopulations. It is suggested that the implied results of the interaction is typical of that between a major predator and one of its less preferred prey. The prominent zonation exhibited by preferred prey, the observed intimacy of association of predator and less preferred prey, and the zoogeographic homogeneity of the Pacific rocky coastline community are discussed in relation to three intermeshing ecological processes.
The seemingly innocent observation that the activities of organisms bring about changes in environments is so obvious that it seems an unlikely focus for a new line of thinking about evolution. Yet niche construction--as this process of organism-driven environmental modification is known--has hidden complexities. By transforming biotic and abiotic sources of natural selection in external environments, niche construction generates feedback in evolution on a scale hitherto underestimated--and in a manner that transforms the evolutionary dynamic. It also plays a critical role in ecology, supporting ecosystem engineering and influencing the flow of energy and nutrients through ecosystems. Despite this, niche construction has been given short shrift in theoretical biology, in part because it cannot be fully understood within the framework of standard evolutionary theory. Wedding evolution and ecology, this book extends evolutionary theory by formally including niche construction and ecological inheritance as additional evolutionary processes. The authors support their historic move with empirical data, theoretical population genetics, and conceptual models. They also describe new research methods capable of testing the theory. They demonstrate how their theory can resolve long-standing problems in ecology, particularly by advancing the sorely needed synthesis of ecology and evolution, and how it offers an evolutionary basis for the human sciences. Already hailed as a pioneering work by some of the world's most influential biologists, this is a rare, potentially field-changing contribution to the biological sciences.
Organisms can receive not only a genetic inheritance from their ancestors but also an ecological inheritance, involving modifications their ancestors made to the environment through niche construction [1
• Laland K.N.
• Sterelny K.
• Odling-Smee J.
• Hoppitt W.
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Cause and effect in biology revisited: is Mayr’s proximate-ultimate dichotomy still useful?.Science. 2011; 334: 1512-1516
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]. Ecological inheritances may persist as a legacy, potentially generating selection pressures that favor sociality. Yet, most proposed cases of sociality being impacted by an ecological inheritance come from organisms that live among close kin and were highly social before their niche construction began [2
• Odling-Smee F.J.
• Laland K.N.
• Feldman M.W.
Niche Construction: the Neglected Process in Evolution. Princeton University Press, Princeton, NJ2003
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]. Here, I show that in terrestrial hermit crabs (Coenobita compressus) — organisms that do not live with kin and reside alone, each in its own shell — niche-construction drives social dependence, such that individuals can only survive in remodeled shells handed down from conspecifics. These results suggest that niche construction can be an important initiator of evolutionary pressures to socialize, even among unrelated and otherwise asocial organisms.
Hermit crabs are critically dependent upon gastropod shells for their survival and reproductive fitness. While anecdotal reports have suggested that hermit crabs may be capable of removing live gastropods from their shells to access the essential shell resource, no systematic experiments have been conducted to investigate this possibility. This paper reports experiments on both marine (Pagurus bernhardus) and terrestrial (Coenobita compressus) hermit crabs in which crabs were paired in the laboratory with the gastropods whose shells they inhabit in the field. Pairings included both shelled and naked crabs and spanned the full range of the gastropod life cycle. Neither marine nor terrestrial hermit crabs were successful at removing live gastropods from their shells. Furthermore, only a small fraction of the crabs (5.7%) were capable of accessing shells in which the gastropod had been killed in advance, with its body left intact inside the shell. Finally, although hermit crabs readily entered empty shells positioned on the surface, few crabs (14.3%) were able to access empty shells that were buried just centimeters beneath them. These results suggest that hermit crabs are constrained consumers, with the shells they seek only being accessible during a narrow time window, which begins following natural gastropod death and bodily decomposition and which typically ends when the gastropod's remnant shell has been buried by tidal forces. Further experiments are needed on more species of hermit crabs as well as fine-grained measurements of (i) the mechanical force required to pull a gastropod body from its shell and (ii) the maximum corresponding force that can be generated by different hermit crab species' chelipeds.
Shell utilization and shell selection studied in the tropical terrestrial hermit crab, Coenobita compressus (H. Milne Edwards). Three major shell related variables are examined; shell size, shell species, and shell condition. Nerita scabricosta (Lamarck) is the most commonly occupied shell, and it is also preferred over other shell species. Coenobita in the field are usually found in smaller than the preferred size of shell, and the difference between utilized and preferred shells is most pronounced in relatively small individuals. Shell size preference differs significantly between similarly sized crabs collected at different sites. There is also a preference for shells which have previously been used by other Coenobita individuals. This preference is due to shell modification by Coenobita, which increases the effective size of the shell. It is argued that the fitness of most sexually mature individuals is probably unaffected by the supply of new shells, since these are too small to be utilized. It is possible that the interaction of adult Coenobita for shells may be better described as mutualism than as competition. This illustrates the fact that a significant difference between utilized and preferred resources need not imply competition for those resources. Results indicate that the nature of intraspecific competition and population regulation in at least this terrestrial hermit crab is significantly different from these processes in marine hermit crabs.
Freilandbeobachtung des Erwerbs von Schalen einer durch Raubschnecken frisch getteten Schnecke durch Einsiedlerkrebse.
Whether animal signals convey honest information is a central evolutionary question, since selection pressures could, in some circumstances, favour dishonesty. A prior study of signalling in hermit crabs proposed that the cheliped extension display of Pagurus bernhardus might represent such an instance of dishonesty. A limitation of this conclusion, however, was that honesty was defined in the context of size assessment, neglecting the potential information that displays might transmit about signallers' variable internal states. Recent analyses of signalling in this same species have shown that its displays provide reliable information about the amount of risk crabs are prepared to tolerate, which therefore might enable signallers to use these displays to honestly convey their motivation to take such risks. Here we test this ‘honest advertisement of motivation’ hypothesis by varying crabs' need for food and analysing their signalling during simulated feeding conflicts against a model. When crabs were starved for 1–5 days, they dropped significantly in weight. Despite this decrement in resource-holding potential and energy reserves, crabs were more likely to perform cheliped extension displays the longer they were food deprived. Longer-starved crabs, whose subjective resource value was greater, also displayed at a higher rate and were more likely to risk seizing the food from the model. We conclude that cheliped extension is a reliable indicator of crabs' internal state and suggest how this honest signal might operate in conflicts over a variety of other resources in addition to food. We propose that future studies detecting apparent dishonesty should analyse many possible signal–state correlations before concluding a signal is actually dishonest.
The symbiotic associates of hermit crabs (excluding parasites and flora) are reviewed worldwide. The review includes species found on the shells occupied by hermit crabs (epibiotic species), species boring into these shells (endolithic species), species living within the lumen of the shell (either free-living or attached to the shell), species attached to the hermit crabs themselves, and hypersymbionts. In total over 550 invertebrates, from 16 phyla are found associated with over 180 species of hermit crabs. Among these associates, 114 appear to be obligate commensals of hermit crabs, 215 are facultative commensals, and 232 are incidental associates. The taxa exhibiting the highest number of associates are arthropods (126), polychaetes (105), and cnidarians (100). The communities of species associated with Dardanus arrosor, Paguristes eremita, Pagurus bernhardus, Pagurus cuanensis, and Pagurus longicarpus are the best studied and harbor the most diverse assemblages of species. While trends in biodiversity of hermit crab assemblages do not follow predicted patterns (e.g., hermit crabs within the Indo-West Pacific do not harbor more species than those from temperate regions), this is suggested to reflect a lack of sampling rather than a true representation of the number of associates. Hermit crabs date to at least the Cretaceous and provided a niche for a number of groups (e.g., hydractinians, bryozoans, polydorids), which were already associates of living gastropods. Apparently hermit crab shells initially supplied a substrate for settlement and then these symbiotic relationships were reinforced by enhanced feeding of symbionts through the activity of the hosts. Through their use and recycling of gastropods shells, hermit crabs are important allogenic ecosystem engineers in marine habitats from the intertidal to the deep sea. Hermit crabs benefit from some symbionts, particularly cnidarians and bryozoans, through extension of shell apertures (alleviating need to switch into new shells) and by providing protection from predators. However, hermit crabs are also negatively impacted (e.g., decreased reproductive success, increased predation) by some symbionts and a review of egg predators is provided. Thus, the symbiotic relationships between hermit crabs and many associates are difficult to characterize and often exhibit temporal changes depending on environmental and biological factors. Research on the biology of these symbionts and the costs/benefits of their associations with hermit crabs are analyzed. While some associates (e.g., Hydractinia spp.) have been studied in considerable detail, for most associations little is known in terms of the impacts of symbionts on hosts, and future experimental studies on the multitude of relationships are suggested.
When interacting organisms have opposing genetic interests, the integrity of communication systems may be undermined. For signaling in such conflict circumstances to remain evolutionarily stable, cheaters must be handicapped. Agonistic threat signals, however, are not always constrained or costly to produce, and yet these signals occur in the severest of conflicts where strong incentives exist for dishonesty. A leading hypothesis for how reliability is stabilized under these conditions is that signaling entails a risk, making signalers vulnerable to injury. Here I experimentally alter vulnerability to show how risk can modify organisms' willingness to escalate disputes, affecting the use of threat signals. The vulnerability to injury of hermit crabs (Pagurus bernhardus) was manipulated by varying the exposure of their soft uncalcified abdomens. When faced with potentially damaging conspecific attacks, more vulnerable crabs were conflict averse, showing reluctance to claim ownership over contestable food, frequently retreating from threats, and refraining from threatening others. The risk an organism can bear in escalated conflict can thus mediate its agonistic behavior and usage of threats. Postural nuances can consequently provide reliable information about aggressive intentions despite minimal production costs and opposing interests between communication parties. Copyright 2007, Oxford University Press.
Shell selection and utilization in a terrestrial hermit crab, Coenobita compressus
ABRAMS, P., 1978. Shell selection and utilization in a terrestrial hermit crab, Coenobita compressus
(H. Milne Edwards). Oecologia, 34: 239-253.