Commensalism

Crinoids shelter a wide variety of species of marine organisms in many symbiotic relationships (Deheyn, D. D et. al, 2006).  Some of the phylum and families that live on or within crinoids include Myzostomida, Decapoda, Galatheidea, Gastropoda, Polychaeta (Deheyn, D. D et. al, 2006). 

The most common two reasons for animals to live symbiotically with crinoids are the ability to hide from predation among the complex morphological structures of feather stars, and the similarity of prey type and feeding mechanism, meaning food capture is easy for the symbiont (Deheyn, D. D et. al, 2006). Many symbiotic inhabitants feed on the plankton that has been trapped by their crinoid hosts (Fabricius, K. E. and Dale, M. B. 1993). Colour similarity between the host crinoid and symbiont have been recorded (Deheyn, D. D et. al, 2006), with many symbionts that live externally on the crinoids being well camouflaged (Fabricius, K. E. and Dale, M. B. 1993).  

  


Crinoid Host-Selection by a Crustacean 

Commensals living on or in crinoids have been shown to have high host-specificity (Fishelson, L., 1974). A species of squat lobater known as the feather star squat lobster, Allogalathea elegans, has shown in many studies to select Capillaster multiradiatus as its primary host (Baeza, J. A. 2011, Encyclopedia of Life, 2018). 

When this specimen of C. multiradiatus was collected from the Gold Coast, an individual A. eleganswas found hiding amongst the feather stars’ arms. Myself, along with colleague Michael, wanted to investigate whether this squat lobster would continuously select C. multiradiatus as its host when given a variety of host options.

Two separate experiments were run to investigate the decision time for host selection, and the frequency of selection. The hypotheses for these experiments were were:

• Decision time: Allogalathea elegans would take the least amount of time to select Capillaster multiradiatus as a host, when only given one choice, and take the longest time to chose the rock as the host
• Selection frequency: Allogalathea elegans select Capillaster multiradiatus as a host more frequently than any other species/object, when able to chose between many hosts, and select the rock least frequently

The decision time experiment was run so that A. elegans would be placed into a container of water with only one host species/object, as shown in figure 5. There were four separate treatments, one with C. multiradiatus, one with only rock, and two sepearte treatments, both with a different Crinoid species, taken from the same location as C. multiradiatus; Lamprometra palmate, and Comaster schlegelii. This is illustrated in the figure below. Time was recorded from when the lobster was released into the water, to when it was in contact with the host for 5 seconds. Time was then average between the 5 trials of each treatment, to give an average time score for each host.

 
Figure 5: The set up of both experiments, with specimens in place

Graph 1 illustrates results from this experiment. As hypothesised, C. multiradiatus had the lowest time score for selection by A. elegans, with a mean time of 88.2 seconds. Following this was C. schlegelii with a mean time of 101.4 seconds, then L. palmate, 116.2 seconds, and finally the rock with a mean time score of 186.0 seconds. 

Graph 1: Graph displaying the average time score for A. elegans to select a particular host species

For the selection frequency experiment, all four host choices were placed in the same large container, at the four corners, shown in figure 5. 16 trials were run, and each time A. elegans was placed in the centre of the container, and timed until it chose a host specimen. Time taken and host chosen were both recorded. Graph 2 shows the results. 


Graph 2: Graph displaying the frequency percentage of trials that A. elegans selected each host species

Results from this experiment were highly unpredicted, with A. elegans chosing C. schlegelii at the highest frequency, 37.5% of the time, followed by the rock, 31.25%, then C. multiradiatus, chosen at a rate of 25.0%, and lastly, only 6.25% of the time was L. palmate selected as host. 

Results from the first experiment confirmed the hypothesis, that C. multiradiatus would be chosen at a faster rate, due to host-specificity between the species, and the response of A. elegans to the rock would be the slowest. These feather star lobsters are almost exclusively known to live within the appendages and on the bodies of feather stars, and with some having only a select few species they will chose to reside in (Baeza, J. A. 2011). 

Surprisingly, when given three species of feather star and one rock to select from, A. elegans chose the rock over 30% of the time. This is quite unusual, given that the complex external morphology of crinoids acts as protection for the symbiont, where they’re able to shelter amongst the arms, pinnules, and cirri (Deheyn, D. D et. al, 2006). The majority of symbionts will find crinoids with colour similarities to themselves, and A. elegans, while not the same colour as C. multiradiatus, was able to successfully camouflage itself amongst the rays, so it is surprising that this species was only selected 25% of the time. 

Crinoids are especially chosen by many symbionts due to the similarity of food items and feeding mechanisms for both host and commensal species (Deheyn, D. D et. al, 2006). Crinoids feed on planktonic particles, and A. elegans also feeds on plankton particles. Furthermore, some symbionts will take food particles from the crinoid, either from its ambulacral groove, or from the mucus secreted by the animal, and eat that as well (Fabricius, K. E. and Dale, M. B. 1993). It is also possible that because of the incredibly artificial setting of this experiment that this isn’t the results that would occur in a natural habitat. 

Predation and regeneration
Crinoids are subject to predation, most commonly from fish, but attacks from echinoderms and other invertebrates has also been documented (Baumiller, T. K., and Gahn, F. G. 2012, Meyer, D. 1985). Since they do not usually move, apart from daily diel transitions, and because they need to be exposure in currents to suspension feed, this leaves them more vulnerable to predators (Baumiller, T. K., and Gahn, F. G. 2012). The majority of attacks are ‘sublethal’, meaning the intensity of the attack is quite low, and death will not occur (Meyer, D. 1985). Most commonly, predators will only graze on pinnules, visceral mass, or potentially parts of arms (Byrne, M., and O'Hara, T. 2017). 

Some attacks by fish are more likely due to the range of commensal species living on the crinoid. Direct attacks on crinoids are rarer than simple grazing, and it has been hypothesised that comatulids may be distasteful to fish (Baumiller, T. K., 2008). Potential adaptations of crinoids to reduce this predatory behaviour include living in cryptic habitats so to hide the oral disc away, having a diel activity pattern, as the vast majority of coral reef fishes feed predominantly during the day, morphological defences including spine-like oral pinnules or dense arms, biochemical defences such as toxic or distasteful compounds, and adaptation to a free-living form with the ability to swim away (Byrne, M., and O'Hara, T. 2017, Meyer, D. 1985). 

Reproduction

All crinoids are gonochoric, whereby the male and female reproductive organs are in separate individuals (Vail, L. 1987). The sexes are indistinguishable apart from gonads with mature gametes which can sometimes be recognised as ovaries or testes (Byrne, M., and O'Hara, T. 2017). The gonads are situated on the ambulacral side of the genital pinnules (Byrne, M., and O'Hara, T. 2017), and all develop asynchronously, with those in the lower quarter of the arm maturing first (Rutman, J. L., and Fishelson, L. 1985). Gonads consist of a genital tuble enclosed in a hemal sinus, which is surrounded by the genital coelom (Ruppert, E. E. et al. 2004).

The reproductive cycle of each gonad includes six stages. Oogonia and spermatoogonia differentiate from the innermost layer of the gonad wall, and as spermatozoa matures and ripens it accumulates in the lumen. Ripening of male gametes is synchronous, while in females ripening is asynchronous (Rutman, J. L., and Fishelson, L. 1985). Along one on an individual, the gonads are in differing stages of development, with the most proximal gonads usually being the most advanced (Rutman, J. L., and Fishelson, L. 1985). Gametes are fertilised externally in most crinoids, and most broadcast their gametes (Byrne, M., and O'Hara, T. 2017). Capillaster multiradiatus has been observed to spawn just after dark (Vail, L. 1987). Spawning occurs by rupturing of the pinnules walls, and gametes then released into the water (Ruppert, E. E., Fox, R. S. and Barnes, R. D. 2004). 

Development

All crinoids have short-lived, non-feeding larvae, beginning with a non-feeding doliolaria that is barrel-shaped and has four or five hoop-like ciliated bands and an anterior apical tuft (Ruppert, E. E. et al. 2004), as shown in figure 6. For a short time, it is free-swimming, but undergoes many morphological changes until settlement on the bottom (Rutman, J. L., and Fishelson, L. 1985). They attach to the substrate via a glandular midventral depression, located near the apical tuft. Metamorphosis then occurs an a benthic, non-feeding, stalked crinoid develops (McEdward, L. R., and Miner, B. G., 2001). Comatulids continue metamorphosis into a stalked, feeding sessile stage, known as a pentacrinoid. Up to several months later, during which time the cirri have formed, the crown releases from the stalk and the young adult comatulid begins living a free-existence (Ruppert, E. E. et al. 2004).

Figure 6: Doliolaria larvae of a crinoid species. Image source: (McEdward, L. R., and Miner, B. G., 2001)

Feeding

Crinoids have been labelled as passive, non-selective suspension feeders that rely on water currents to bring food to them (Byrne, M., and O'Hara, T. 2017, Meyer, D. L. 1982). However, they do play an active role in modifying their arm and pinnule posture, aligning their arm fans to be normal to the current, and mobile feather stars can seek areas with better conditions for feeding (Byrne, M., and O'Hara, T. 2017). Comatulids anchor their cup to the substrate and extend their arms in a half circular ‘fan’ (Baumiller, T. K., 2008). Capillaster multiradiatusdoesn’t form a true filtration fan, but still extends its arms from the central point and responds to tidal current flows over the reef (Meyer, D. I., 1979). 

During feeding the arms are outstretched with the tube feet upright (Ruppert, E. E. et al. 2004). The tube feet bear mucus-secreting papillae, which assist in food capture (Rutman, J., and Fishelson, L., 1969), and occur in a series of triplets (Ruppert, E. E. et al. 2004). The primary tube foot is the longest, and all primary feet on one pinnule create a food-catching mesh. From the feet, food is transferred to the ambulacral groove and to the mouth to be ingested (Ruppert, E. E. et al. 2004). Its believed that food capture is only limited by the ambulacral groove width and activity of the prey (Meyer, D. L. 1982). However, food particles much larger than groove width in C. multiradiatushave been recorded in stomach contents (Byrne, M., and O'Hara, T. 2017). 

The length and spacing of the tube feet has been found to influence position of a species within the reef (Meyer, D. I., 1979). Species with longer and more widely spaced tube feet are more likely to live within in structure of the reef, and hold their arms in a multidirectional posture (Meyer, D. I., 1979). Those with tube feet that shorter and spaced closer together tend to position themselves in exposed positions and form complete filtration fans (Meyer, D. I., 1979). 

C. multiradiatusfeeds only at night, so emerges roughly one hour before sunset from its daytime hiding place amongst crevices in the reef (Meyer, D. L. 1982). It feeds at lower levels, along side formations of the reef, and will select its habitat for optimal current conditions (Baumiller, T. K., 2008). The main diet of crinoids includes detritus, benthonic microorganisms, and plankton that is ‘raining down’ (Rutman, J., and Fishelson, L., 1969). One study of the stomach of C. multiradiatusfound the following contents: sediment grains: 32.6%, phytoplankton: 32.5%, Protozoa: 20.1%, Mollusca:2.0%, Crustacea: 1.5%, miscellaneous 3.9% (Meyer, D. L. 1982). 

Stalkless comatulids have the ability to move freely, and are capable or swimming or crawling within their habitat (Ruppert, E. E., Fox, R. S. and Barnes, R. D. 2004). Movement is always with the oral surface facing up. To crawl around the substratum, comatulids can lift their body up and move around on the downward-flexed arms. They often use the small, terminal hooks on their arms and pinnules to grasp surfaces (Ruppert, E. E., Fox, R. S. and Barnes, R. D. 2004). 

Despite their ability to do so, most movement, particularly swimming, is usually only an escape response (Ruppert, E. E., Fox, R. S. and Barnes, R. D. 2004). The highest observed usual movement is of nocturnal species, such as C. multiradiatus, that move between hiding crevices and feeding areas between day and night.

Body Form

Crinoids have skeletons that are composed of numerous thick, vertebra-like ossicles, giving their appendages a jointed appearance (Ruppert, E. E. et al. 2004). This skeleton is bound with ligament and muscle, and is organised into three body parts: a cup, that holds most of the vital organs, arms, that area arranged radially around this cup, and a stalk, which elevates the cup above the ground (Baumiller, T. K., 2008). 

As juveniles, C. multiradiatus starts with a central mouth, but during postlarval development the mouth migrates to a marginal position on the tegmen (Summers, M. M. et. al, 2017, Clark, A. H. 1921). The anus is also present on the tegmen, on the oral (upward facing) side of crinoids, often at the summit of an anal cone, elevating it above the feeding current (Ruppert, E. E. et al. 2004). 

Symmetry

Like all species in the phylum Echinodermata, crinoids exhibit pentamerous symmetry, meaning their body can be divided into five similar sections from the central axis (Ruppert, E. E. et al. 2004). However, their larvae display a bilateral symmetry (McEdward, L. R., and Miner, B. G., 2001) which is lost through shifting of the body axis of the individual and through torsion (Ruppert, E. E. et al. 2004).

Arms, Pinnules and Ambulacral Grooves

The arms of Capillaster multiradiatus radiate from the pentamerous crown; whilst primitive species usually only have 5 arms, the base of most crinoids bifurcate and create a total of 10 arms. Further branching along these arm radials can create the appearance of multiple arms (Ruppert, E. E. et al. 2004). C. multiradiatuscan have over 100 arms on one individual. Each arm consists of a series of small articulated plates known as brachials, and a group of these brachials between branchings of the arm are called brachitaxis (Oji, T. and Okamoto. T., 1994). 

Figure 8: Illustration of a 'semi-exploded' view of the proximal portion of a feather star. Picture adapted from Ruppert, E. E. et. al 2004.

On each arm is a bilaterial series of pinnately arranged pinnules (Ruppert, E. E. et al. 2004), giving the feather stars’ arms their feather look, and its also its common name. Crinoids also possess modified pinnules that perform different tasks within the individual. Some pinnules are specialised ‘genitals’ that bear the gonads, whilst other pinnules located near the base of the rays are the oral pinnules that can be modified for protecting and cleaning the tegmen (Byrne, M., and O'Hara, T. 2017). The oral pinnules are mechano-receptive and ambulacra or tube feet, and can almost completely cover the disc to protect it (Alender, C.B. et al. 1966). The pinnules also give the species its ‘sticky’ feeling, due to the many proximally-directed hooks on the middle and distal pinnules (Byrne, M., and O'Hara, T. 2017). 

Five ambulacral grooves, seen in figure 9, are present on the tegmen and these extend onto the oral surface of both the arms and pinnules. These grooves have margins with movable flaps (called lappets), which allow it to be open or closed (Ruppert, E. E. et al. 2004). Food particles are transported down the grooves to the mouth by three tube feet located on the inner side of each lappet (Fatherree, J. W. 2013, Ruppert, E. E. et al. 2004). The arms, pinnules, and ambulacral grooves are all not only used in feeding, but also are used for locomotion (Byrne, M., and O'Hara, T. 2017). 

Figure 9: Arrows pointing to the ambulacral gores on the arms of Capillaster multiradiatus 

 

Tube Feet   

The tube feet, also known as podia, are small, sticky extensions of the water vascular system located in the ambulacral grooves of echinoderms (Baumiller, T. K., 2008), seen in figure 10. However, unlike others in that phylum, crinoids’ tube feet lack a terminal sucker. Yet, they can still act as an adhesive filter (Byrne, M., and O'Hara, T. 2017) by producing mucous threads used in suspension feeding (Rutman, J., and Fishelson, L., 1969). C. multiradiatus have roughly six tube feet per mm, and each are an average length of 07.mm (Meyer, D. I., 1979). 

Figure 10: Tube feet extending out of the ambulacral groove of a pinnule on the arm of Capillaster multiradiatus

Cirri

Cirri are root-like projections from the bottom of the theca (part of the crown) on the centrodorsal of crinoids, shown in figure 11. Stalkless comatulids use the cirri instead of the stalk to attach the cup to substrate (Baumiller, T. K., 2008). In C. multiradiatus they are typically less than 25mm long, and made up of less than 25 segments known as cirrals (Messing, C. G., 2003). They are non-feeding appendages that are used only for attachment and not locomotion, like they can be in some species of comatulids (Fishelson, L., 1974). 

Figure 11: The cirri of Capillaster multiradiatus extending from the bottom of the crown

Water Vascular System

All echinoderms possess a water vascular system (WVS), and the crinoid WVS is very similar (Ruppert, E. E. et al. 2004). It is a collection of fluid-filled tubes and bladders, ending in numerous tube feet, and supports respiration and circulation (Fatherree, J. W. 2013). However, crinoids WVS has two main differences to the rest of the phylum; they lack a madreporite, and stone canals.  Instead of a madreporite, often hundreds of tegmenal pores are present on the oral surface that lead into the perivisceral coelom. The ring canal gives rise to the stone canals which also lead into the perivisceral coelom (Ruppert, E. E. et al. 2004). It’s most likely that seawater enters via the perivisceral coelom and tegmenal pores and then is pumped into the WVS by the stone canals (Ruppert, E. E. et al. 2004). 

From the central ring canal, a radial canal enters each one of the arms and extends a lateral canal into each pinnule (Ruppert, E. E. et al. 2004). The radial canals parallel the ambulacral grooves along the arms (Byrne, M., and O'Hara, T. 2017). Hydraulic pressure is generated by contracting muscle fibres connecting to the radial canal. This extends the tube feet which are situated off the lateral canals (Ruppert, E. E. et al. 2004). 

Mutable tissue

Echinoderms have the ability to change the mechanical properties of connective tissues in their body, within just a few seconds (Wilkie, I. 2002). Mutable collagenous tissue (MCT) is present in some of the connective tissue of crinoids, meaning they’re able to adjust properties such as viscosity, stiffness, and tensile strength through active neural control (Baumiller, T. K., 2008). While the dermis contains muscles, nerves, and other cell types, its within the extracellular matrix that this stiffening occurs. There are two types of nerves present within the extracellular matrix, one that hardens and another that softens, and it appears that changes in calcium affect these nerves (Ruppert, E. E. et al. 2004).

This function is highly important; by stiffening structures such as their arms, crinoids are able to withstand high external forces, and destiffening means their body can move with minimal force (Baumiller, T. K., 2008). Crinoids can maintain their posture, particularly during feeding, by stiffening the MCT, and use a lot less energy than if they were to do so with muscle (Baumiller, T. K., 2008). 

Body wall and Musculature

Crinoids have both a cuticle and an epidermis surrounding their body. The epidermis is only ciliated in the ambulacral grooves (Ruppert, E. E. et al. 2004). Below the epidermis is a connective-tissue layer that is continuous with the deeper connective tissue in the body. The cirri, arms, and pinnules are almost solid, filled with a series of thick, vertebra-like ossicles (Ruppert, E. E. et al. 2004).

Distinct musculature is confined mainly to the arms and pinnules (Ruppert, E. E. et al. 2004). Obliquely striated flexor muscles that run between the proximal edges of the arm and the pinnule ossicles flex the arms and pinnules and make them curl (Ruppert, E. E. et al. 2004). Muscular articulations allow mobility between the plates of the arms, meaning the arms can have flexible movement (Oji, T. and Okamoto. T., 1994). This is incredibly important as a crinoids’ arms perform feeding, and locomotion. 

Ossicles of the arms are joined together by ligaments or muscles and ligaments (Byrne, M., and O'Hara, T. 2017). Contraction causes the arm to bend inwards (Byrne, M., and O'Hara, T. 2017), and elastic recoil of the interbrachial ligaments causes extension of the appendages (Ruppert, E. E. et al. 2004) When the muscles relaxes, ligaments can become rigid and allow the arm to maintain its extended feeding posture with little energy expenditure (Byrne, M., and O'Hara, T. 2017). 

Identification of the species 

Many different reports have been published regarding correct identification of feather stars (Clark, A. H. 1921, Pawson, D. L. 1972, Rowe, F. W. E, et. el. 19860. However, Summers et. al. 2017 produced a succinct and clear table outlining the diagnostic morphological characteristics of species in Comatulidae. They highlighted some of the main identification points, including an excentric mouth (not central), first syzygy at 3+4 on arms arising from IBr, and comb teeth that are single, triangular, confluent with outer edge of pinnule, and not tapering significantly distally, or tapering to a blunt tip (Summers, M. M. et. al 2017). 

 


Table 1: Table explaining the diagnostic morphological characteristics of Capillaster multiradiatus. Image source: (Summers, M. M. et. al, 2017)

A syzygy is “where radiating ridges and grooves on the two joint faces appose each other so that the external suture resembles a perforated line” (Byrne, M., and O'Hara, T. 2017). Crinoids are modular and their skeletons have several repeated parts along their arms, so some of their forms are abbreviated (Byrne, M., and O'Hara, T. 2017). The abbreviation br is used for and individual brachial (one individual piece of skeleton), brachitaxes are abbreviated to Br, proceeded by a roman numeral indicating its position from the base of the ray, and followed by a number indicating the number of component ossicles (Byrne, M., and O'Hara, T. 2017). If a + is present, it indicates that there is a syzygy present between those two ossicles. For example, IIBr 4(3+4) indicates that this is the second brachitaxes on the arm (branching has occurred once), that there are four ossicles present in this brachitaxes, and that there is a syzygy between brachial three and four. 

Having IIBr 4(3+4) is actually one of the species identifiers of Capilaster multiradiatus, the first syzygy at 3+4 on arms arising from IBr (from the second brachitaxes). Figure 12 demonstrates this syzygy. 

Figure 12: The syzygy at IIBr 4(3+4) and the entire IIBr brachitaxes of the Capillaster multiradiatus specimen 

Another identifiable characteristic is that of triangular, confluent, and exterior comb teeth on the pinnules, shown in figure 13.  



Figure 13: A pinnule of Capillaster multiradiatus showing the comb teeth as triangular, confluent, and ending at a blunt tip

Digestive System 

After food particles are caught by the tube feet and mucus and moved into the ambulacral groove, cilia transport it towards the mouth. It reaches the digestive system which is contained in the central disc, including a mouth, that leads into the oesophagus, and then into the intestine. The intestine does a complete circle around the inside of the calyx wall and then passes back up into the rectum and out of the anus (Ruppert, E. E. et al. 2004). 

Circulation

The perivisceral coelom is the main circulatory system within a crinoid, and exists in the central disc, arms, and pinnules (Ruppert, E. E. et al. 2004). Within the central disc, it surrounds the gut and the axial organ, which is a large blood vessel that holds epithelial tubes. Branches from this coelom enter the arms where a bilateral pair of oral coelomic cavities and unpaired aboral cavities exists. A branch from one oral and one aboral cavity extend into the pinnule united by canals. Flow is outbound from the disc in the aboral cavity, and inbound in the oral cavity (Ruppert, E. E. et al. 2004).

The oral hemal ring is the centre of the hemal system, and this gives rise to the axial organ and a network of hemal vessels in the coelomic mesenteries. Crinoids do not have a heart and the blood is colourless, yet the axial still organ pulses (Ruppert, E. E. et al. 2004).

Respiration and excretion

There is little information regarding respiration of crinoids, all that is known is that the tube feet are the primary sites of gas exchange. The large surface area of the arms means that any special respiratory surfaces are not required. There is also no special excretory organs of crinoids currently known(Ruppert, E. E. et al. 2004). 

Autotomy and Regeneration

Crinoids have the ability to cast off a part of their body and then regenerate those parts back (Baumiller, T. K., and Gahn, F. G. 2012). Loss of body parts, including the appendices (arms, pinnules, cirri) and internal organs or whole visceral mass, can occur via self induced loss or by physical disturbances, wave action, entanglement, or unfavourable conditions causing stress.  In some experiments, crinoids have been able to regenerate their body parts even when the body was halved, or reduced to only one fifth (Carnevali, C. 2006). 
 

The nervous system plays an important role in regeneration, and some of the main cellular elements responsible for the regrowth of appendices and visceral mass include amoebocytes, coelomocytes, granulocytes, phagocytes (Meyer, D. 1985). Autotomy and subsequent regeneration are very important when crinoids are dealing with predation (Baumiller, T. K., 2008) with regeneration occurring quite quickly after disturbance events (Meyer, D. 1985).

Larvae are also able to undergo partial regeneration of some parts of their body, but it isn’t a commonly recorded event (Carnevali, C. 2006). 

Capillaster multiradiatus lost many pinnules and segments of arms during this observational period, and showed incredibly quick regeneration of two new arms, as seen in figure 14. 

 

Figure 14: Two new arms growing from one of the radials of the central disc of Capillaster multiradiatus