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Clibanarius taeniatus
Yellow Striped Hermit Crab


Candice Selmanovic 2016

Summary

Clibanarius taeniatus, commonly known as the yellow-striped hermit crab, is a member of the suborder anomura. Distinguished by its yellow and green longitudinal colouring, C. taeniatus is a common species of hermit crab found in mud flats, rock pools and sandy intertidal zones along the north and east Australian coast, and south east coast of Papua New Guinea. C. taeniatus can sometimes be confused with the yellow-footed hermit crab, Clibanarius virescens, as they are regularly found in the same areas competing for food and shells. Although they have similar yellow and green colourings, they can be distinguished as C. taeniatus has longitudinal colouring along its appendages and upper body, while C. virescens is dark green/brown all over with yellow colouring only on distal ends of its appendages. 

The two specimens investigated were found on mudflats at low tide, on North Stradbroke Island, off the east-coast of Queensland, Australia. In order to more closely analyse their movements and interactions, the specimens were observed and photographs taken of some of these appendages. Further supplementary research was also undertaken in order to understand the complex life-history, behaviour and  anatomy and physiology more thoroughly. 

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Figure 1

Physical Description

C. taeniatus is a relatively small species of hermit crab, recognisable by its distinguished colouring. Growing up to 35-40mm outside of its shell (Queensland Museum, 2016), the yellow-striped hermit crab remains true to its common name, with dark green and yellow longitudinal stripes along its legs, claws and upper body. Like most hermit crabs, C. taeniatus finds and utilises empty gastropod shells to armour its non-calcified abdomen and protect itself from predation. This soft abdomen is unsegmented, and usually twisted to the right in healthy individuals (Lancaster, 1988). 

As with all crustaceans, hermit crabs are biramous. They have two sets of antennae, with the smaller set located proximal to the eye stalks and referred to as the antennulae.  In order to hold its mobile shelter in place, the fourth and fifth setae covered pereiopods are reduced and used as struts to maintain its position inside the shell (Brichtwell, 1951). Likewise, the telson and uropods are used as hooks and anchors to hold onto the interior of the shell (See Figure 2 and 3) (Brichtwell, 1951). Furthermore,  hermit crabs possess the ability to move forward in a straight line, as opposed to the side-ways “crab-walk” usually adopted by the true crabs.

Sexual dimorphism in favour of males is common in many hermit crab species, including in C. taeniatus (Turra, 2004; Martinelli, Mantelatto & Fransozo, 2002). Abrams (1988) has hypothesised three reasons for this sexual dimorphism. The first being that males are able to expend more energy into growth as they do not need energy for egg production, thus making them larger, faster. The second hypothesis is that larger males can fertilise many females, so greater reproductive potential is correlated with larger size. The third and final hypothesis is that intraspecific fights for  the opportunity to copulate with females is more likely to be won by larger males. While its possible that just one of these hypotheses are the reason for sexual dimorphism in hermit crabs, it is more likely that a combination of two, or all of them play a role. 

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Figure 2
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Figure 3

Ecology

Diet

Best described as “omnivorous detritivores” (Lancaster, 1988), hermit crabs are opportunistic in their feeding habits, which may be a contributor to their success inhabiting unpredictable, often extreme environments (Lancaster, 1988). Common food acquisition methods include filtering, deposit feeding, scrapping or scrubbing detritus from small and large surfaces, and even predation (Dunbar, 2002). Filter feeding often involves using modified “feathered antennae” to capture food from the water and transfer to the mouth (Dunbar, 2002). Alternately, the setae of the maxillipeds may also be used to filter suspended food material, which is then brushed toward the mouth (Lancaster, 1988). Deposit feeding involves using the chelipeds, and sometimes the walking legs, to “scoop” material to the hair covered 3rd maxillipeds (Dunbar, 2002; Lancaster, 1988). These “hairs” -the setae-  on these maxillipeds then act as a brush, transferring food material to the crabs mouth (Lancaster, 1988).  

While detritus is the main source of food and nutrients for hermit crabs (Hazlett, 1981), species including Birgus latro Gecarcinidae natalis and Cardiosoma hirtipes, among others (Dunbar, 2002) have also been known to predate upon much larger prey than themselves (Lancaster, 1988). Such prey includes ophiuroids, bivalves, amphipods and crangonids (Lancaster, 1988). Cannibalism has also been observed in some species including and includes smaller hermit crabs and sometimes even their own body parts that have been damaged, crushed  or completely removed (Lancaster, 1988).

In C. taeniatus , observations of gut contents of has revealed they mainly feed on soft detritus including decayed seagrass and its associated fauna and epiphytic algal flora (Kunze & Anderson, 1979). The abundance of epiphytes found in gut contents of C. taeniatus leads researchers to suggest that this is its preferred food over seagrass (Kunze & Anderson, 1979). In C. taeniatus,   epiphytes are collected by using the chelipeds to scrape surface of sea grass (Kunze and Anderson, 1979).  Macrophagous feeding on dead plant and animal material is not as common in C. taeniatus than in some other species of hermit crab (Kunze & Anderson, 1979).

Habitat and Predators

Hermit crabs are generally very successful inhabitors of a wide range of habitat types including coral reef crests and flats, intertidal zones and rocky tide pool areas. C. taeniatus  however is found predominantly in both sandy and rocky intertidal, tide pool areas and mudflats (see Figure 4)  (Dunbar, 2002).

As one of the smaller species of hermit crab and as a result of its relatively exposed habitat, C. taeniatus is predominantly predated upon by birds, though in high tide these may extend to include elasmobranchs, octopus and some mantis shrimp and bony fish (Williams & McDermott, 2004). It is also thought that the feeding and reproductive strategies of some species of flatworms result in predatory behaviours on the eggs of hermit crabs (Williams & McDermott, 2004). These flatworms cement their egg masses to the inside of the host hermit crabs shell and have been confused with the gonadal mass of the hermit crab (Williams & McDermott, 2004). Though they aren’t thought to harm the brooding female host, these flatworms do reduce the reproductive potential as a result of this egg/embryo predation, but do no affect the males of the species (Williams & McDermott, 2004). 


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Figure 4

Life History and Behaviour

Reproduction and Development

Little research has been completed regarding the specific reproduction and development strategies of C. taeniatus, however the reproductive routine undertaken by copulating pairs of hermit crabs is generally consistent between species, with few variations. Furthermore, reproduction usually varies seasonally, though it can occur year round, and the peaks of reproduction seem to vary by magnitude depending on the latitude (Hazlett, 1981).

Like most decapods, hermit crabs including C. taeniatus are gonochoric, with two distinct sexes, although some may be hermaphroditic (Turra, 2004). Copulation is stimulated by female pheromones, resulting in males becoming more active and seeking out females (Shepherd & Edgar, 2013). Once a female is located, the male grasps the females shell with his walking legs and the pair engage in a brief foreplay before they both emerge from their shells (Shepherd & Edgar, 2013). Here the mating pair expose their ventral surfaces to one another, with the male on top, and the spermatophore is transferred to the female on her third or fourth pereiopod (see Figure 5) (Lancaster,  1988). Spawning occurs just hours after fertilisation and after exiting through the females gonophore, the developing embryos then move to the abdomen and attach to the females enlarged pleopods (Hess & Bauer, 2002). Females release their mature eggs into the water column by gently but repeatedly rocking the abdomen in and out of their shells, and the resulting larvae remain planktonic for a few weeks (Shepherd & Edgar, 2013).

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Figure 5

Anatomy and Physiology

Morphology and appendages of the hermit crab Clibanarius taeniatus

Anomurans are characterised by having reduced fourth and fifth pairs of pereiopods, a second set of antennae outside of the eyestalks and by being carapace-free on the ventral side of the last thoracic plate (Lancaster, 1988). Unlike many other invertebrate taxa, hermit crabs and other decapods have exceptionally complex and numerous appendages, of which each order has specialised in a different manner. 


Figure 6 displays a median view of C. taeniatus from the right. The right-side coiling of the soft, unprotected abdomen is clear in this image, highlighting how vulnerable these animals are without their protective shells. The long uniramous antennae is also obvious, with the smaller, biramous antennulae visible in Figure 7, proximal to the antennae and compound eye stalks. The antennae contain a statocyst at their base and the nephridiopore (not pictured). The statocyst is hollow, and densely lined with mechanoreceptive cells, allowing the animal to sense its orientation as it moves, based on the earths gravitational pull (Ruppert, Fox & Barnes, 2004). The antennae are also often used to direct water currents for food collection and respiration. 

The first pair of pereiopods are enlarged, forming the chelipeds. They create a pincer, or a type of opposable fingers, with one side closing against the other to grab food, shells or a mate. Pereiopods two and three are uniramous, and used in the forward walking motion of anomurans. Chelipeds can sometimes also be used to aid walking. At the end of the coiled abdomen is the uropod, which forms a kind of hook when inside the shell to hold itself in place. Likewise, the reduced fourth pereiopod in Figure 7 is not normally visible when inside the shell and is covered in setae which both help keep itself in place when inside the shell. 

Figure 8 shows an alternate view of C. taeniatus, fully displaying the fused thoracic carapace. The branchiostegite (gill chamber) is also visible here, and a stylised version of the inside of the gill chambers can be viewed in Figure 10c. 

Finally, the mouthparts of C. taeniatus in Figure 9 shows the complexity of the feeding behaviours of hermit crabs. It requires these complex external mouthparts, maxillipeds, chelipeds and the internal proventriculus to all integrate functionally (Kunze & Anderson, 1979). While the degree of involvement of these complex parts differs, the importance of each is no less. Interestingly in C. taeniatus, the second and third walking pereiopods also help to stir up detrital layers, which their associated setae then collects. It is however more common for detrital material to be scooped up by the chelipeds and then transferred via the second and third maxillipeds to the inner mouth (Kunze & Anderson, 1979). The chelipeds are also commonly used to scrape epiphytic algae, thought to be C. taeniatus preferred food. While in larger individuals of C. taeniatus food material may be held to the mandibles and torn apart, it is more common for this species to take part in the more passive, sedentary mode of feeding (Kunze & Anderson, 1979). In this manner, when detritus and algae is abundant, they will rest their shell on the substrate and use just their third maxillipeds to collect food (Kunze & Anderson, 1979). The endopods of these appendages are rapidly flexed in no particular pattern to shift the food matter towards the first and second maxillipeds, where the food material is sorted and then ingested (Kunze & Anderson, 1979).

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Figure 6
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Figure 7
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Figure 8
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Figure 9

Internal Transport and Excretion

Unlike most other invertebrates, decapods have a very well developed hemal system which comprises a heart, well-developed arterial system as well as capillaries and venous sinuses (Ruppert, Fox & Barnes, 2004). The heart has evolved from its primitive tubular morphology, and comprises a rectangular sac in the thorax (Ruppert, Fox & Barnes, 2004). Though it consists of a single chamber, its location, suspended in the pericardial cavity, acts as a second chamber (; McMahon & Burnett, 1990).  Since this system is an open system there is no direct venous return of hemolymph, instead it returns to the pericardial cavity, where three paired ostia return the hemolymph back to the heart. (McMahon & Burnett, 1990). Scientists have estimated complete circulation in large decapods to take just 40 to 60 seconds total (Ruppert, Fox & Barnes, 2004). Though relatively simple in design, this system is able to regulate and control the flow of hemolymph between all organs and tissue beds, in addition to providing the role of the lymphatic system (Ruppert, Fox & Barnes, 2004).

While most decapods are able to excrete nitrogenous waste across their highly permeable gill epithelia, their hemolymph coelomic cavity also allows the possession of a single excretory pore (Ruppert, Fox & Barnes, 2004). These are known as antennal glands, and are located at the base of the second antennae. This gland, the nephridiopore, is connected to a proximal labyrinth, which maintains the bloods ionic balance. This in turn is connected to a distal bladder, which stores urine and has a short duct connecting it directly to the nephridiopore for excretion (Ruppert, Fox & Barnes, 2004). 

Gas Exchange

In decapods, up to 24 pairs of gills associated with the thoracic appendages provide the gas exchange requirements (Ruppert, Fox & Barnes, 2004). The gills are very well perfused and highly permeable due to the very thin gill cuticle surrounding them. This leave the gills highly permeable to both the gases required for respiration, but also to a variety of other materials and ions that may be present in the water (Ruppert, Fox & Barnes, 2004). As with all crabs, the water enters the gill chambers at the base of the chelipeds (Ruppert, Fox & Barnes, 2004). The setae located at the base of the chelipeds filters the incoming sea water, removing sediment from the flow, before moving through to the gill chambers via a current created by the gill bailer (See Figure 10a and 10c) (Ruppert, Fox & Barnes, 2004). The gill bailer is paddle-like, beating to form the current, directing the incoming water to flow lateral across the gill filaments, then exiting through the exhaling apertures  via an anterior flow (Ruppert, Fox & Barnes, 2004). The passage of water through the gill chamber follows a U shape (see Figure 10b). In decapods like C. taeniatus,  the three elongated epiopods of the maxillipeds sweep the gill filaments, cleaning them of foreign particles to maximise the countercurrent oxygen exchange (Ruppert, Fox & Barnes, 2004).

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Figure 10

Biogeographic Distribution

C. taeniatus is a relatively common species across Australia, found in mudflats and intertidal zones from Shark Bay, Western Australia, to Port Hacking, New South Wales (see Figure 11). It has also been recorded throughout the eastern, Indo-West Pacific region, on the south-east coast of Papua New Guinea.

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Figure 11

Evolution and Systematics

C. taeniatus arises from the phyla arthropoda, the largest metazoan group which contains approximately 80% of all extant animal species (Ruppert, Fox & Barnes, 2004).All taxa within the phyla arthropoda can be characterised by a number of features, including segmentation, paired, jointed appendages, a chitinous skeleton and an absence of locomotory ciliation (Ruppert, Fox & Barnes, 2004). 

The subphylum crustacea is a sister taxa to the mandibulata (Ruppert, Fox & Barnes, 2004). Crustacea contain more morphological and ecological heterogeneity than any other animal taxon, and utilise their numerous appendages well with a variety of specialisations within the taxa (Rupprt, Fox & Barnes, 2004). They are recognisable immediately by their two pairs of antennae and are usually separated  into two or more tagmata (Ruppert, Fox & Barnes, 2004). Their heads consist of five fused segments, bearing five paired appendages (Ruppert, Fox & Barnes, 2004). 

Within the crustacea is the class malacostraca, of which hermit crabs and a number of other well known crustaceans belong. Their  thorax and abdomen have a combined number of 19 segments- eight for the thorax and always six for the abdomen, plus the telson (Ruppert, Fox & Barnes, 2004). Primitive malacostracans included seven abdominal segments however this had fused and reduced to six segments in most of todays taxa. Their appendages are not only paired, but also usually biramous, which can aid feeding, movement, ventilation, creating a feeding current, brooding eggs or gas exchange (Ruppert, Fox & Barnes, 2004). 

The order decaopda contains approximately one quarter of the known crustaceans, and are usually the most well known of the crustaceans. Within the decapoda in the infraorder anomura, of which the transition from shrimp-like decapods to true crabs is believed to be occurring (Ruppert, Fox & Barnes, 2004). These taxa are characterised by having a moderately reduced abdomen and reduced fifth legs (Ruppert, Fox & Barnes, 2004). The anomura are mostly hermit crabs, which are further belonging to the superfamily, paguroidea (Ruppert, Fox an Barnes, 2004). It is believed that the hermit crabs ancestral condition utilised crevices and holes for protection, leading to the loss of the hard ,calcified abdomen (Ruppert, Fox & Barnes, 2004). Today, most anomurans seek out discarded gastropod shells to allow safe mobility, while others may be enclosed in the base of an anemone (Ingle & Christiansen, 2004).

Conservation and Threats

C. taeniatus is not currently listed on the IUCN Red List of Threatened Species (IUCN, 2016), and  sources and research on this species have not indicated difficulty in finding this species in its natural habitat, despite its small size (Dunbar, 2002; Kunzel & Anderson, 1979).

While C. taeniatus does not appear to be associated with any immediate conservation issues, research in this area highlights the necessity for available and appropriate gastropod shells for hermit crabs to procure in order to protect themselves from predators and physical stressors (Abrams, 1988; Hazlitt, 1981; Dunbar, 2002, Bertness, 1981). These shells already have limited availability, leading to both inter and intraspecific competition for those available (Bertness, 1981). Thus, the collection of shells by humans for recreational purposes may negatively impact the density and survivability of these crabs, should these practises become intense enough (Bertness, 1981). Athough C. taeniatus is more successful and abundant in coastal areas than other species of hermit crab where freshwater inundation has occurred (Dunbar, Coates & Kay, 2003), other forms of habitat destruction and modification, particularly in coastal regions, may pose a threat to this species, as with most animals whose habitat is in close proximity to humans.

References

Abrams, P. A. 1988. 'Sexual difference in resource use in hermit crabs: consequences and causes. In Behavioural adaptation to intertidal life (ed. G. Chelazzi and M. Vannini)', pp. 283-296. NewYork: Plenum, Inc.

Bertness, M. D. 1981, ‘Pattern and plasticity in tropical hermit crab growth and reproduction’, The American Naturalist, vol. 117, no. 5, pp. 754-773. 

Brichtwell, L. R. 1951, ‘Some experiments with the Common Hermit Crab, (Eupagurus bernhardus)  Linn., and transparent univalve shells’,  Proceedings of the Zoological Society of London, vol. 121, pp. 279-283.

Dunbar, S. G. 2002, ‘Respiratory, osmoregulatory and behavioural determinants of distribution of two tropical marine hermit crabs’, PhD Thesis, Central Queensland University, Rockhampton.  

Dunbar, S. G., Coates, M., & Kay, A. 2003, ‘Marine hermit crabs as indicators of freshwater inundation on tropical shores’, Memoirs of Museum Victoria, vol. 60. no. 1, pp. 27-34.

Hazlett, B. A. 1981, ‘The behavioural ecology of hermit crabs’, Annual Review of Ecology and Systematics, vol. 12, pp. 1-22.

Hazlett, B. A. 1972, ‘Shell fighting and sexual behaviour in the hermit crab genera Paguristes and Calcinus, with comments on Pagurus,’ Bulletin of Marine Science, vol. 22, pp. 807-823.

Hess, G. S. & Bauer, R. T. 2002, 'Spermatophore transfer in the hermit crab Clibanarius vittatus (crustacea, anomura, diogenidae)’, Journal of Morphology, vol. 253, no. 2, pp. 166-175.

Ingle, R. W & Christiansen, M. E. 2004, Lobsters, mud shrimps and anomuran crabs , Synopses of the British fauna (New Series)no. 55, Field Studies Council, Shrewsbury. 

Kunze, J. & Anderson, D. T. 1979, ‘Functional morphology of the mouthparts and gastric mill in the hermit crabs Clibanarius taeniatus (Milne Edwards), Clibanarius virescens (Krauss), Paguristes squamosus McCulloch and Dardanus setifer (Milne-Edwards) (Anomura: Paguridae)’, Australian Journal of Marine and Freshwater Research, vol 30, pp. 683-722.

Lancaster, I. 1988, ‘Pagurus bernhardus (L.) – an introduction to the natural history of hermit crabs’, Field Studies, vol. 7, pp. 189-238.

Martinelli, J. M., Mantelatto, F. L. M. & Fransozo, A, 2002, ‘Population structure and breeding season of the south Atlantic hermit crab, Loxopagurus loxochelis (Anomura, Diogenidae) from the Ubatuba Region, Brazil’, Crustaceana, vol. 75, no. 6, pp. 791-802.

McMahon, B. R. & Burnett, L. E. 1990, ‘The crustacean open circulatory system: a reexamination’, Physiological Zoology, vol. 63, pp. 35-71.

Queensland Museum, 2016, Yellow Striped Hemit: Clibanarius taeniatus, viewed 25 May 2016, <http://www.qm.qld.gov.au/Find+out+about/Animals+of+Queensland/Crustaceans/Common+marine+crustaceans/Hermit+Crabs+Squat+Lobsters+and+allies/Yellow-striped+Hermit#.V0aIkZN97e0>.

Ruppert, E. E., Fox. R. S., & Barnes. R. D, 2004, Invertebrate Zoology: A Functional Evolutionary Approach, 7th edn, Brooks/Cole, Belmont, USA.

The Atlas of Living Australia, 2016, Clibanarius taeniatus (H. Milne Edwards, 1848), viewed 25 May 2016, <http://bie.ala.org.au/species/CLIBANARIUS%20TAENIATUS>.

Shepherd, S. A., & Edgar, G. J, 2013, Ecology of Australian Temperate Reefs: the Unique South, CSIRO Publishing, Collingwood, Victoria. 

Turra, A, 2004, ‘Intersexuality in hermit crabs: reproductive role and fate of ionophores in intersex individuals’, Journal of the Marine Biological Association of the United Kingdom, vol. 84, pp. 757-759.

Williams, J. D., & McDermott, J. J. 2004, ‘Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates,’ Journal of Experimental Marine Biology and Ecology, vol. 305, pp. 1-128.