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Discipline
Biological
Keywords
Living Space
Limiting Resource
Competition
Observation Type
Standalone
Nature
Case study
Submitted
Apr 8th, 2019
Published
Jun 3rd, 2019
  • Abstract

    Living space is a fundamental resource for the growth and survival of plants, marine, and terrestrial animals and even human beings. Of the variety of life that covert space, hermit crabs are unique in their motivation to find, defend and maintain gastropod shells as portable homes. The limited supply of empty shells in the environment, as well as a constant need to upgrade these resources as they grow, means that these charismatic crabs are always on the lookout for bigger, better and newer homes. We present the curious case of an intertidal hermit crab (Isocheles sawayai) that was found dead, tucked away behind the body of an injured gastropod (Olivancillaria vesica) whose shell it was presumably trying to occupy. This unusual observation highlights the extremes to which some crabs may go to beat potential rivals and be the first to access limiting resources.

  • Figure
  • Introduction

    Living space can take the form of competitor-free substrate (e.g., barnacles), physical refuge (e.g., urchins and reef fish), territory or home ranges (e.g., wolves) or even physical extensions to body-form (e.g., shelled organisms like mussels). Of all the animals that covert living space, hermit crabs (Paguroidea) are unique in their use of empty gastropod shells as a secure living space to protect their soft abdominal exoskeleton.

    Having a good-quality shell is not only essential for continued growth, but is vital to protect individuals against predation, desiccation, thermal and osmotic stress. Because of this, hermit crabs have evolved the ability to rapidly assess the quality of a potential shell (i.e., its subjective value;), which in turn dictates many aspects of their behaviour including: competitive interactions with other individuals (shell fights;) and the unusual phenomenon of aggregating at shell exchange markets. The vital need to upgrade shells throughout their lives means that hermit crabs are constantly on the lookout for bigger, better, and more spacious homes.

    To increase the chances of encountering a suitable empty shell, hermit crabs use a range of tactics including: random locomotion, attendance at shell-supplying sites (where shells may be sourced or traded) and aggressive interactions with conspecifics. Often the challenge is made more difficult because of the critically limited supply of these resources. This has been previously acknowledged along the southern Atlantic coast of Brazil and is thought to be the reason crabs utilize gastropod shells of a wide range of shapes and sizes (i.e., up to 17 different species). More recently, such limitation has been reflected in observations of hermit crabs utilizing a range of unusual shelters (e.g., barnacles and bivalves) and even plastic debris derived from a certain brand of chocolate egg. Such clear scarcity in limiting resources can drive crabs and other organisms to attempt exploitation of resources that can have adverse effects on fitness and survival.

  • Objective

    In this short article, we present a curious case of resource exploitation that highlights the extremes to which hermit crabs may go to be the first to access limiting shell resources. During recent biodiversity surveys at Palmeiras Beach in Caraguatatuba Bay (Brazil), a hermit crab (Isocheles sawayai) was observed dead, tucked away behind the body of a still living but injured gastropod (Olivancillaria vesica). Here we report on this curious incident and consider the possible causes and implications for hermit crab populations in shell limiting environments.

  • Results & Discussion

    Upon collection, the body of the deceased hermit crab was almost completely obscured by the foot of the still living gastropod (Fig. 1A). Upon closer in situ inspection, the dactylus and the propodus of the second and third pereopods of the crab were found to be sticking out between the shell aperture and the gastropod foot (this species of gastropod does not have an operculum). Although still alive, the foot of the gastropod showed signs of a failed predation attempt, most likely from a species of large swimming crab known to use a tactic called ‘peeling’ that can lead to non-lethal injuries. Figure 1(B-C) presents the extraction sequence for the hermit crab in the laboratory. The shield length (a most common measure of size) of the hermit crab was 5.8 mm, while the shell internal volume was 10 mL, making it a large and particularly desirable home if not occupied by the body of the gastropod.

    Isocheles sawayai is a filter-feeding hermit crab that lives partially buried in sandy substrates within shallow coastal waters. Although has been shown to inhabit the empty shells of Olivancillaria vesica it is not the preferred domicile shell species in sheltered environments (i.e., 5.6% of observations). In the surf zone, however, as was the case in the study area, these shells can act as a ballast for hermit crabs preventing burial and overturning by waves.

    This is the first observation of a hermit crab is found dead inside the shell of a still-living gastropod that we could find in the published literature. This is surprising given that there have been decades of targeted work investigating the ecology of a range of common benthic intertidal species (including Isocheles sawayai). While there is no way to know exactly how this curious incident came about, there are two plausible explanations. First, the crab searching for a replacement shell, encountered the live gastropod and preyed upon it in an attempt to secure its shell. Although our literature review revealed some species of hermit crabs have been shown to attack live gastropods in the laboratory, this has never been reported for this species or indeed any other group in nature. The second explanation is that like many other hermit crabs, this individual was attracted by the smell of the injured gastropod (almost certainly the result of a failed predation event) and climbed into the mantle cavity of the gastropod – as hermit crabs typically do when evaluating or exchanging shells. Subsequently, and while attempting to remove the remaining tissue, the individual became trapped by the contracting foot and was subsequently suffocated.

    Although we will never know definitively how this curious incident occurred, it highlights the pitfalls of acquiring resources in limiting environments and is interesting from a perspective of marine ethology and evolutionary biology. Greater sampling within the study area may provide evidence on whether this is an isolated instance or whether it might be a more common phenomenon exhibited by this and perhaps other species of the hermit crab. It would also be interesting to evaluate if other hermit crabs (some of which live in extremely shell limiting environments) may engage in similar extreme behavior to be the first to access limited resources. Globally, it will become increasingly important to understand the responses of animals to decreasing resource availability within marine and coastal environments.

  • Conclusions

    This curious incident involving a hermit crab and a gastropod highlights the pitfalls of acquiring resources in limiting environments and may have parallels for other organisms that covert space to survive and thrive.

  • Conjectures

    Greater sampling within the study area may provide evidence on whether this is an isolated instance or whether it might be a more common strategy exhibited by this species of the hermit crab. It would also be interesting to evaluate if other hermit crabs (some of which live in extremely shell limiting environments) may engage in this type of activity. Globally, it is going to become increasingly important to understand the potential responses to decreasing resource availability in intertidal environments.

  • Methods

    The collection site was Palmeiras Beach, Caraguatatuba Bay (23º40’04.84S, 45º25’49.60W), located on the southeast coast of Brazil in the state of São Paulo. As part of intertidal surveys done for a study into the population biology of the trigonal clam (Tivela mactroides) a range of specimens were sampled from intertidal quadrats along a wave-swept shore. The observation described in this short article involved a specimen of the hermit crab Isocheles sawayai [Forest & de Saint Laurent, 1968] and a typically non-preferred gastropod Olivancillaria vesica [Gmelin, 1791]. This hermit crab is a filter feeding infra-littoral species that lives partially buried in sandy substrates within shallow coastal waters along the western Atlantic coast, from Venezuela to Brazil (Santa Catarina). Upon discovery, the two organisms were photographed and preserved in ethanol (70% in seawater) for transportation to the benthic laboratory where the crab was extracted and properly identified. A subsequent literature analysis was undertaken to identify previous descriptions of this phenomena for this particular species and intertidal hermit crabs more generally.

  • Funding statement

    The São Paulo Research Foundation (FAPESP) provided support for the production of this article through a research grant to DG (2018/06162-6).

  • Acknowledgements

    Laboratory work was done at the Center for Marine Biology, University of São Paulo (CEBIMar).

  • Ethics statement

    Not applicable.

  • References
  • 1
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    Matters12.5/20

    The curious incident of the hermit crab and the gastropod

    Affiliation listing not available.
    Abstractlink

    Living space is a fundamental resource for the growth and survival of plants, marine, and terrestrial animals and even human beings. Of the variety of life that covert space, hermit crabs are unique in their motivation to find, defend and maintain gastropod shells as portable homes. The limited supply of empty shells in the environment, as well as a constant need to upgrade these resources as they grow, means that these charismatic crabs are always on the lookout for bigger, better and newer homes. We present the curious case of an intertidal hermit crab (Isocheles sawayai) that was found dead, tucked away behind the body of an injured gastropod (Olivancillaria vesica) whose shell it was presumably trying to occupy. This unusual observation highlights the extremes to which some crabs may go to beat potential rivals and be the first to access limiting resources.

    Figurelink

    Figure 1. Extraction of the dead hermit crab (Isocheles sawayai) from behind the foot of a gastropod (Olivancillaria vesica) still in its shell.

    (A) In situ condition as discovered in the field.

    (B–D) The gradual removal of crab from the lower basal margin of the gastropod foot.

    Note: The anterior of the shell points toward the right-hand side of the frame.

    Introductionlink

    Living space can take the form of competitor-free substrate (e.g., barnacles[1]), physical refuge (e.g., urchins and reef fish[2][3]), territory or home ranges (e.g., wolves[4]) or even physical extensions to body-form (e.g., shelled organisms like mussels[5]). Of all the animals that covert living space, hermit crabs (Paguroidea) are unique in their use of empty gastropod shells as a secure living space to protect their soft abdominal exoskeleton[6].

    Having a good-quality shell is not only essential for continued growth[7], but is vital to protect individuals against predation[8], desiccation, thermal[9] and osmotic stress[10]. Because of this, hermit crabs have evolved the ability to rapidly assess the quality of a potential shell (i.e., its subjective value;[11]), which in turn dictates many aspects of their behaviour including: competitive interactions with other individuals (shell fights;[12]) and the unusual phenomenon of aggregating at shell exchange markets[13][14]. The vital need to upgrade shells throughout their lives means that hermit crabs are constantly on the lookout for bigger, better, and more spacious homes.

    To increase the chances of encountering a suitable empty shell, hermit crabs use a range of tactics including: random locomotion, attendance at shell-supplying sites (where shells may be sourced or traded) and aggressive interactions with conspecifics[13]. Often the challenge is made more difficult because of the critically limited supply of these resources[15]. This has been previously acknowledged along the southern Atlantic coast of Brazil and is thought to be the reason crabs utilize gastropod shells of a wide range of shapes and sizes (i.e., up to 17 different species[16]). More recently, such limitation has been reflected in observations of hermit crabs utilizing a range of unusual shelters (e.g., barnacles and bivalves[17]) and even plastic debris derived from a certain brand of chocolate egg[18]. Such clear scarcity in limiting resources can drive crabs and other organisms to attempt exploitation of resources that can have adverse effects on fitness and survival.

    Objectivelink

    In this short article, we present a curious case of resource exploitation that highlights the extremes to which hermit crabs may go to be the first to access limiting shell resources. During recent biodiversity surveys at Palmeiras Beach in Caraguatatuba Bay (Brazil), a hermit crab (Isocheles sawayai) was observed dead, tucked away behind the body of a still living but injured gastropod (Olivancillaria vesica). Here we report on this curious incident and consider the possible causes and implications for hermit crab populations in shell limiting environments.

    Results & Discussionlink

    Upon collection, the body of the deceased hermit crab was almost completely obscured by the foot of the still living gastropod (Fig. 1A). Upon closer in situ inspection, the dactylus and the propodus of the second and third pereopods of the crab were found to be sticking out between the shell aperture and the gastropod foot (this species of gastropod does not have an operculum). Although still alive, the foot of the gastropod showed signs of a failed predation attempt, most likely from a species of large swimming crab known to use a tactic called ‘peeling’ that can lead to non-lethal injuries[19]. Figure 1(B-C) presents the extraction sequence for the hermit crab in the laboratory. The shield length (a most common measure of size) of the hermit crab was 5.8 mm, while the shell internal volume was 10 mL, making it a large and particularly desirable home if not occupied by the body of the gastropod.

    Isocheles sawayai is a filter-feeding hermit crab that lives partially buried in sandy substrates within shallow coastal waters[20]. Although has been shown to inhabit the empty shells of Olivancillaria vesica it is not the preferred domicile shell species in sheltered environments (i.e., 5.6% of observations). In the surf zone, however, as was the case in the study area, these shells can act as a ballast for hermit crabs preventing burial and overturning by waves.

    This is the first observation of a hermit crab is found dead inside the shell of a still-living gastropod that we could find in the published literature. This is surprising given that there have been decades of targeted work investigating the ecology of a range of common benthic intertidal species (including Isocheles sawayai[16]). While there is no way to know exactly how this curious incident came about, there are two plausible explanations. First, the crab searching for a replacement shell, encountered the live gastropod and preyed upon it in an attempt to secure its shell. Although our literature review revealed some species of hermit crabs have been shown to attack live gastropods in the laboratory[21], this has never been reported for this species or indeed any other group in nature. The second explanation is that like many other hermit crabs[22], this individual was attracted by the smell of the injured gastropod (almost certainly the result of a failed predation event) and climbed into the mantle cavity of the gastropod – as hermit crabs typically do when evaluating or exchanging shells. Subsequently, and while attempting to remove the remaining tissue, the individual became trapped by the contracting foot and was subsequently suffocated.

    Although we will never know definitively how this curious incident occurred, it highlights the pitfalls of acquiring resources in limiting environments and is interesting from a perspective of marine ethology and evolutionary biology. Greater sampling within the study area may provide evidence on whether this is an isolated instance or whether it might be a more common phenomenon exhibited by this and perhaps other species of the hermit crab. It would also be interesting to evaluate if other hermit crabs (some of which live in extremely shell limiting environments) may engage in similar extreme behavior to be the first to access limited resources. Globally, it will become increasingly important to understand the responses of animals to decreasing resource availability within marine and coastal environments.

    Conclusionslink

    This curious incident involving a hermit crab and a gastropod highlights the pitfalls of acquiring resources in limiting environments and may have parallels for other organisms that covert space to survive and thrive.

    Conjectureslink

    Greater sampling within the study area may provide evidence on whether this is an isolated instance or whether it might be a more common strategy exhibited by this species of the hermit crab. It would also be interesting to evaluate if other hermit crabs (some of which live in extremely shell limiting environments) may engage in this type of activity. Globally, it is going to become increasingly important to understand the potential responses to decreasing resource availability in intertidal environments.

    Methodslink

    The collection site was Palmeiras Beach, Caraguatatuba Bay (23º40’04.84S, 45º25’49.60W), located on the southeast coast of Brazil in the state of São Paulo. As part of intertidal surveys done for a study into the population biology of the trigonal clam (Tivela mactroides) a range of specimens were sampled from intertidal quadrats along a wave-swept shore. The observation described in this short article involved a specimen of the hermit crab Isocheles sawayai [Forest & de Saint Laurent, 1968] and a typically non-preferred gastropod Olivancillaria vesica [Gmelin, 1791]. This hermit crab is a filter feeding infra-littoral species that lives partially buried in sandy substrates within shallow coastal waters along the western Atlantic coast, from Venezuela to Brazil (Santa Catarina)[20]. Upon discovery, the two organisms were photographed and preserved in ethanol (70% in seawater) for transportation to the benthic laboratory where the crab was extracted and properly identified. A subsequent literature analysis was undertaken to identify previous descriptions of this phenomena for this particular species and intertidal hermit crabs more generally.

    Funding Statementlink

    The São Paulo Research Foundation (FAPESP) provided support for the production of this article through a research grant to DG (2018/06162-6).

    Acknowledgementslink

    Laboratory work was done at the Center for Marine Biology, University of São Paulo (CEBIMar).

    Conflict of interestlink

    The authors declare no conflicts of interest.

    Ethics Statementlink

    Not applicable.

    No fraudulence is committed in performing these experiments or during processing of the data. We understand that in the case of fraudulence, the study can be retracted by ScienceMatters.

    Referenceslink
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      Free space availability and larval substratum selection as determinants of barnacle population structure in a developing rocky intertidal community
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      Fighting for shells: how private information about resource value changes hermit crab pre-fight displays and escalated fight behaviour
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      Spatial and temporal variation in the predation risk for hermit crabs in a subtropical bay
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      Journal of the Marine Biological Association of the United Kingdom, 58/1978, pages 869-876 DOI: 10.1017/s0025315400056824chrome_reader_mode
    11. Alexander Turra, Daniel Gorman
      Subjective resource value and shell abandoning behavior in hermit crabs
      Journal of Experimental Marine Biology and Ecology, 452/2014, pages 137-142 DOI: 10.1016/j.jembe.2013.12.018chrome_reader_mode
    12. Gareth Arnott, Robert W. Elwood
      Information gathering and decision making about resource value in animal contests
      Animal Behaviour, 76/2008, pages 529-542 DOI: 10.1016/j.anbehav.2008.04.019chrome_reader_mode
    13. Elena Tricarico, Francesca Gherardi
      Shell acquisition by hermit crabs: which tactic is more efficient?
      Behavioral Ecology and Sociobiology, 60/2006, pages 492-500 DOI: 10.1007/s00265-006-0191-3chrome_reader_mode
    14. Estevão C. F. de Souza, Daniel Gorman, Fosca P. P. Leite, Alexander Turra
      Olfactory selectivity in intertidal hermit crabs: aggregation behavior by Pagurus criniticornis (Decapoda, Anomura) in response to simulated predation on the gastropod Cerithium atratum
      Hydrobiologia, 772/2016, pages 31-43 DOI: 10.1007/s10750-015-2621-6chrome_reader_mode
    15. Richard R. Vance
      Competition and Mechanism of Coexistence in Three Sympatric of Intertidal Hermit Crabs
      Ecology, 53/1972, pages 1062-1074 DOI: 10.2307/1935418chrome_reader_mode
    16. Fantucci M Z, Biagi R, Mantelatto F L
      Shell occupation by the endemic western Atlantic hermit crab Isocheles sawayai (Diogenidae) from Caraguatatuba, Brazil
      Brazilian Journal of Biology, 68/2008, pages 859-867 DOI: 10.1590/s1519-69842008000400023chrome_reader_mode
    17. Garcia R. B., Meireles A. L., Mantelatto F. L.
      Unusual shelters occupied by Brazilian hermit crabs (Crustacea: Decapoda: Diogenidae)
      Brazilian Journal of Biology, 63/2003, pages 721-722 DOI: 10.1590/s1519-69842003000400020chrome_reader_mode
    18. João P. Barreiros, Osmar J. Luiz
      Use of plastic debris as shelter by an unidentified species of hermit crab from the Maldives
      Marine Biodiversity Records, 2/2009, page e33 DOI: 10.1017/s1755267208000377chrome_reader_mode
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      Predation on gastropods by shell-breaking crabs: effects on shell availability to hermit crabs
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      Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites
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