March 2011 Christina Ball Royal BC Museum Phil Lambert GLOSSARY FOR THE ECHINOIDEA

The Echinoidea, similar to other echinoderm groups, have an ancient lineage dating back approximately 500 million years and includes the sea urchins, sand dollars and heart urchins. Today this globally distributed group comprises approximately 1000 species (Pearse et al. 2007). Nine species are known to occur in British Columbia (Lambert and Boutillier in press). Echinoids are found exclusively in the marine environment from the intertidal down into deep water and can be found on rocky, sandy or muddy substrates (Brusca and Brusca 1990).

The echinoids have a variety of body shapes ranging from disc-like sand dollars to pyramidal deepwater species. While their morphology of the echinoids varies, the group shares several other characteristics. The echinoids have mutable collagenous tissue and a water vascular system. They also have a hard endoskeleton, called a test, that is made up of interlocking plates formed from fused ossicles. They have spines and pincher- like pedicellariae that attach to the outer surface of the test and a complex jaw structure called an Aristotle’s Lantern (Lambert and Austin 2007). There is also considerable colour variation within the Echinoidea. While colour can be a useful method for identifying otherwise similar species it is important to recognize that colour is a subjective trait. There can also be considerable colour variation within a species.

Like all echinoderms the echinoids posses a unique tissue type called mutable collagenous tissue. This tissue can change rapidly, in less then a second to several minutes, from a rigid to a flaccid state. The change in physical state, from hard to soft or vice versa is not the result of muscle activation. Rather it is the result of chemical changes to the passive mechanical properties of the tissue itself. The current consensus is that in essence, mutable collagenous tissue is made up of discrete collagen fibrils that are organized into bundles (Wilkie 2002). Substances released by the juxtaligamental cells change the cohesion between the bundles causing the tissue to either harden or soften (Wilkie 2002). These changes are under the control of the nervous system.

The water vascular system is a complex network of canals and reservoirs that uses hydraulic pressure and muscular action to operate the podia (Brusca and Brusca 1990). In echinoids the podia, or tube feet, are primarily used for locomotion, attachment and gas exchange (Brusca and Brusca 1990; Lambert and Austin 2007). The water vascular system opens to the surrounding sea water via a plate called the madreporite. The echinoids have a fairly obvious madreporite on the aboral surface.

In all types of echinoid the hard test is formed from a series of interlocking plates that are themselves formed from fused calcareous ossicles. The two types of plates, ambulacral and interambulacral, run in longitudinal rows from the mouth to the anus. Rows of ambulacral plates alternate with rows of interambulacral plates. The ambulacral plates have small holes (pores) through which the tube feet extend (Brusca and Brusca 1990; Lambert and Austin 2007). The pores occur in pairs and the number and arrangement of the pore pairs is important for identifying specimens (figure 1).

1 March 2011 Christina Ball Royal BC Museum Phil Lambert On the outside of the test are tubercles to which the spines attach. At the center of the tubercle is a ball-like mamelon that is the articulation point for the spine. Mamelons may be either perforate (i.e. have a small hole in the middle) or not. The neck of the mamelon is either straight or undercut (Lambert and Austin 2007). A parapet surrounds the mamelon and can be either crenulated (i.e. wavy like a crown) or smooth and flat. Muscles surrounding each mamelon attach the spine to the test and control its movements. Both the tubercles and spines can be useful when identifying specimens. In cross section the spines are made up of a series of wedges (figure 1), the number of which is characteristic of a particular species.

a b

Figure 1. The arrangement of pore pairs in Strongylocentrotus franciscanus (a), and a cross section of a primary spine of S. fragilis showing the spine wedges (b.

The echinoids also have pedicellariae, which attach to small tubercles on the outer surface of the test (Lambert and Austin 2007). The pedicellariae are used in defense, to clean debris off the surface of the test and to capture prey (Brusca and Brusca 1990; Lambert and Austin 2007). Pedicellariae are pincher- or jaw-like structures on flexible stalks (figure 2). There are three types of pedicellariae (ophicephalous, tridentate and globiferous, figure 2) and any given species might have two or more types. Within the different types of pedicellariae the shape of the three-part jaw and stalk can vary (Lambert and Austin 2007). The shape of the pedicellariae and its stalk can be important identifying features for some echinoids.

Figure 2. Three types of echinoid pedicellariae: ophicephalous from Strongylocentrotus droebachiensis (a), tridentate from S. droebachiensis (b), tridentate from S. franciscanus (c), and globiferous from S. droebachiensis (d). Parts of a pedicellaria (e).

2 March 2011 Christina Ball Royal BC Museum Phil Lambert The mouth is located on the side of the test facing the substrate. The anus is located opposite the mouth in the urchins, but shifted posteriorly in the sand dollars and heart urchins (Pearse et al. 2007). The area surrounding the anus is termed the periproct. All of the Echinoidea have a complex jaw structure called an Aristotle’s Lantern. It is shaped like an old fashioned lantern and is made up of five teeth, muscles and levers. The ends of the teeth protrude from the mouth (Brusca and Brusca 1990; Lambert and Austin 2007; Pearse et al. 2007). The echinoids use these teeth to cut up food, rasp algae off of rocks, and to build burrows.

a b

c

Figure 3. Morphology of a typical sand dollar (a), heart urchin (b), and sea urchin (c).

Most of the echinoids have two separate, though outwardly indistinct, sexes (Brusca and Brusca 1990; Lambert and Austin 2007). The regular echinoids have five gonads each leading into its own gonoduct. The irregular echinoids (e.g. sand dollars and heart urchins) have four gonads and a corresponding number of gonoducts (Brusca and Brusca 1990). Each gonoduct leads to a gonopore (opening) on the genital plate. The genital plates are located on the aboral surface near the anus (Lambert and Austin 2007).

Eggs and sperm are released from the gonads and exit through the gonopores into the water where the sperm fertilize the eggs (Brusca and Brusca 1990; Lambert and Austin 2007). While in the water column the embryo develops into a bilaterally symmetrical larva. After 4-6 weeks the larva undergoes metamorphosis into a tiny juvenile urchin and settles onto suitable habitat (Lambert and Austin 2007). As an

3 March 2011 Christina Ball Royal BC Museum Phil Lambert alternative strategy a few echinoids carry and brood their young between their spines (Brusca and Brusca 1990).

The Echinoidea inhabit a range of trophic niches. Most urchins are omnivorous grazers and scavengers that scrape algae and encrusting animals off hard surfaces. For example the familiar Purple Urchin consumes kelp and algae as well as encrusting animals and detritus (Lambert and Austin 2007). Some species use their teeth to build burrows in hard substrates. The animals scrape algae off the sides of the burrow or catch algae that drifts into the burrow (Brusca and Brusca 1990).

Most of the irregular echinoids are detritivores. Some irregular urchins burrow into soft sediment and feed on organic particles. These species usually use their tube feet to search the sediment for food particles that they then pass to their mouths (Durham et al. 1980; Lambert and Austin 2007). Sand dollars are characterized by a highly modified Aristotle’s Lantern with non-protractible teeth (Lambert and Austin 2007). Most sand dollars are detritivores and particulate feeders that pick-up food particles from the substrate and pass them with their tube feet to the mouth (Telford and Mooi 1996).

While most sand dollars are detritivores and particulate feeders, a few suspension feeders exist. For example Dendraster excentricus, a common sand dollar in BC, catches diatoms and other small food particles with its tube feet and then passes the food to the mouth (Francisco and Herka 2010). It can also use its pedicellariae to catch tiny swimming crustaceans (Brusca and Brusca 1990). In calmer waters this species is usually found with the anterior portion of the body buried in the substrate and the rest of the body protruding out of the substrate at an angle. In rougher waters the species tend to lie flat on the ground (Durham et al. 1980; Francisco and Herka 2010).

In turn echinoids are predated upon by sea otters, crows, gulls, large fish, sea stars and large crabs (Lambert and Austin 2007; Snellen et al. 2007). Humans are among the most effective predators of sea urchins and can dramatically decrease their populations (Pfister and Bradbury 1996; Lambert and Austin 2007). Some small animals are parasites on urchins. For example parasitic copepods use their mouthparts to pierce the skin and suck out body fluids (Lambert and Austin 2007). Other animals, such as tube worms, scale worms, ostracods and small shrimp often hiding among the spines of urchins.

The echinoids exhibit some interesting behaviour. Many urchins use their tube feet to hold small stones, shells and other objects on top of themselves. The exact reason for this behaviour is uncertain, but it is thought that it could confer several benefits (Lambert and Austin 2007). The covering behaviour could serve as a means of food storage or protect the urchins from desiccation, visible and UV light, predation or dislodgement by strong waves. For example the Green Sea Urchin will cover itself in response to light and wave action (Dumont et al. 2007). The Antarctic sea urchin Sterechinus neumayeri covers itself with kelp that shields it from predation by a sea anemone (Amsler et al. 1999). These examples and other available evidence suggest that different species cover themselves for different reasons (Dumont et al. 2007; Sigg et al. 2007).

4 March 2011 Christina Ball Royal BC Museum Phil Lambert

SPECIES OF BRITISH COLUMBIA AND ADJACENT AREAS This key includes the echinoids known to occur in British Columbia and adjacent areas. Nine species of echinoids are known to occur in British Columbia. Of these, seven are sea urchins, one is a sand dollar and one is a heart urchin. An additional five deep sea species are known to occur to the north or south of BC (indicated with an asterisk) and are expected to or may possibly occur here (Lambert and Boutillier, in press). Four deep sea species (indicated with a cross) are not included in the key as their distribution, generally known from only a few samples, is outside the geographic range covered by this key.

Cidaroida Cidaridae †Aporocidaris fragilis Agassiz and Clark, 1907 †Aporocidaris milleri Agassiz, 1898 Echinothurioida Echinothuriidae Sperosoma biseriatum Doderlein, 1901 *Sperosoma giganteum Agassiz and Clark, 1907 Echinoida Strongylocentrotidae Strongylocentrotus droebachiensis (Müller, 1776), Green Sea Urchin Strongylocentrotus fragilis Jackson, 1912, Pink Sea Urchin Strongylocentrotus franciscanus (Agassiz, 1863), Red Sea Urchin Strongylocentrotus pallidus (Sars, 1871), White Sea Urchin Strongylocentrotus purpuratus (Stimpson, 1857), Purple Sea Urchin Clypeasteroida Dendrasteridae Dendraster excentricus (Eschscholtz, 1831), Pacific Sand Dollar Holasteroida Urechinidae †Cystechinus loveni Agassiz, 1898, Pyramid Sea Urchin Pourtalesiidae *Ceratophysa ceratopyga valvaecristata Mironov, 1976 *Cystocrepis setigera (Agassiz, 1898) Echinocrepis rostrata Mironov, 1973 †Pourtalesia tanneri Agassiz, 1898 *Pourtalesia thomsoni Mironov, 1976 Spatangoida Schizasteridae Brisaster latifrons (Agassiz, 1898), Heart Urchin Aeropsidae *Aeropsis fulva (Agassiz, 1898), Oblong Sea Urchin

5 March 2011 Christina Ball Royal BC Museum Phil Lambert GLOSSARY OF TERMS

Aboral surface – The side opposite to the mouth. In the echinoids this refers to the top side of the body.

Ambulacral Plate – In the echinoids these plates are found between the interambulacral plates. The ambulacral plates are associated with the water vascular system and have pores to allow the tube feet to penetrate the test.

Ampulla – The ampulla is a bulb-like reservoir at the base of a tube foot. The contraction of the ampulla causes the tube foot to extend, much like squeezing one end of a balloon causes the other end to swell.

Aristotle’s Lantern – The five-sided jaw apparatus found only in the Echinoidea. It is made up of five plate-like teeth and numerous ligaments, muscles and levers.

Asexual – A form of reproduction that does not involve the gametes of two separate individuals. Asexual reproduction usually results in offspring that are clones of the parent.

Benthic – Pertaining to the benthos or bottom of a body of water. Benthic organisms live on or in the substrate.

Cilia – Cilia are hair-like structures, found in many groups of invertebrates, which though their movement create small water currents.

Coelom – A fluid filled cavity inside the mesoderm.

Commensal – An organism that lives in close association with another species but does not provide benefits to the other organism or cause it harm.

Conspecific – The term conspecific refers to other members of the same species. For example in a congregation of sea urchins the members of species ‘A’ would all be conspecific to one another. The members of species ‘A’ would be heterospecific to members of species ‘B’.

Distal – The portion of an organism located away from the central axis or disc of an organism.

Endoskeleton – An internal skeleton covered by skin and muscles. Vertebrates and some invertebrates have endoskeletons.

Epidermis – This is the outermost layer of tissue, (i.e. the skin) and forms a barrier between the organism and the outside environment.

Exoskeleton – An external skeleton. Some invertebrates, such as the arthropods, have exoskeletons.

6 March 2011 Christina Ball Royal BC Museum Phil Lambert

Gonads – The sex organs; testis in the male, ovaries in the female.

Gonopore – In echinoderms, the opening in the body wall through which eggs and sperm are released.

Hermaphrodite – An organism that has both male and female sex organs. Hermaphrodites can have both male and female sex organs at the same time (simultaneous hermaphrodite). Alternatively they can change from being a male to a female, or vice versa, over the course of their life (sequential hermaphrodite).

Heterospecific – Members of different species. For example in a congregation of sea urchins the members of species ‘A’ would be heterospecific to members of species ‘B’.

Interambulacral Plate – In the echinoids these plates are found between the rows of ambulacral plates. There are no pores for tube feet in the interambulacral plates.

Juxtaligamental Cells – Special cells in echinoderms that are associated with, and control, through their secretions, mutable collagenous tissue.

Mamelon – The ball-like articulation of a tubercle to which the spines attach. These are found only in the Echinoidea.

Madreporite – A perforated ossicle through which water enters the water vascular system.

Mesoderm – Mesoderm is the middle of the three basic tissue layers in an organism. Some invertebrates (i.e. jelly fish) do not have mesoderm.

Morphology – The overall shape of an organism and the structure of its parts.

Mutable Collagenous Tissue – This type of tissue is found only in the echinoderms and can rapidly change from a soft to a rigid state. The change in state is due to changes in the physical nature of the tissue, mediated by the juxtaligamental cells. The nervous system controls the mutable collagenous tissue.

Oral surface – The side of an organism that contains the mouth.

Ossicle – A single calcified element of an echinoderm endoskeleton.

Pedicellariae – Small pincher-like structures that occur on the outside of many echinoderms. They consist of a muscular stem with a jaw-like head (usually three jaws).

Pelagic – Relating to or living in the middle layers of the water column (i.e. not on the bottom and not at the surface).

7 March 2011 Christina Ball Royal BC Museum Phil Lambert Pentaradial symmetry – A type of radial symmetry, characteristic of echinoderms, in which body parts are arranged along five rays of symmetry.

Periproct – The periproct is the region of softer tissues surrounding the anus in the echinoids. This region also includes the madreporite.

Peristome – The peristome is the region of softer tissues surrounding the mouth in the echinoids. It is located centrally in the regular urchins and off-center in the irregular urchins.

Podia – Another name for tube feet.

Proximal – Close to center of the disc or central axis of an organism.

Radial Canal – The radial canals are part of the water vascular system and branch off the ring canal. The radial canal occurs internally and adjacent to the ambulacral furrow or plate.

Ring Canal – The ring canal is part of the water vascular system and surrounds the mouth.

Sedentary – Organisms that lead a sedentary lifestyle have the ability to move, though often only very slowly, but normally do not move. For example, suspension feeding sea cucumbers are usually sedentary, only moving to reach areas with better water currents or to evade predators.

Suspension Feeding – Suspension feeding is sometimes called filter feeding. Animals that suspension feed strain food particles out of the water using specialized structures and/or a mucus coating.

Tube Feet – In the echinoderms these are hollow, cylindrically shaped extensions of the water vascular system that function in respiration, locomotion and food collection.

Test – The hard spherical or semi-spherical skeleton of a sea urchin. The test is made up of many small plates made of fused ossicles.

Ventral – Usually the lower part of a bilaterally symmetrical invertebrate animal closest to the substrate.

Water Vascular system – A system of water filled canals and chambers that uses hydraulic pressure and muscle contractions to operate the tube feet.

8 March 2011 Christina Ball Royal BC Museum Phil Lambert REFERENCES

Amsler, C.D., J.B. McClintock and B.J. Baker. 1999. An Antarctic feeding triangle: defensive interactions between macroalgae, sea urchins and sea anemones. Marine Ecology Progress Series. 183:105-114.

Brusca, R.C. and G.J. Brusca. 1990. Phylum Echinodermata. Pp. 801-839. In Invertebrates. Sunderland: Sinauer Associates, Inc

Dumont, C.P., D. Drolet, I. Deschênes and J.H. Himmelman. 2007. Multiple factors explain the covering behaviour in the green sea urchin, Strongylocentrotus droebachiensis. Animal Behaviour. 73: 979-986.

Durham, J.W., C.D. Wagner and D.P. Abbott. 1980. Echinoidea: the sea urchins. Pp. 160-170. In Intertidal invertebrates of California edited by R.H. Morris, D.P. Abbott and E.C. Haderlie. Stanford: Stanford University Press.

Francisco, V. and S.Z. Herzka. 2010. Regulation of feeding mode by the sand dollar Dendraster excentricus in a shallow estuarine habitat. Journal of Experimental Marine Biology and Ecology. 383: 146-155.

Kozloff, E.N. 1996. Class Echinoidea. Pp 459-460. In Marine invertebrates of the Pacific Northwest. Seattle and London: University of Washington Press.

Lambert, P. and W.C. Austin. 2007. Royal British Columbia Museum handbook: brittle stars, sea urchins and feather stars of British Columbia, southeast Alaska and Puget Sound. Victoria: Royal British Columbia Museum.

Lambert, P. and J. Boutillier. In press. Deep Sea Echinodermata of British Columbia. Canadian Technical Reports of Fisheries and Aquatic Sciences.

Pearse, J.S., R. Mooi, C. Mah, C.G. Messing, G. Hendler and P. Lambert. 2007. Echinodermata. Pp. 913-948. In The Light and Smith manual: Intertidal invertebrates from central California to Oregon edited by J.T. Carlton. Berkley and Los Angeles: University of California Press.

Pfister, C.A. and A. Bradbury. 1996. Harvesting red sea urchins: recent effects and future predictions. Ecological Applications. 6(1): 298-310.

Sigg, J. E., K. M. Lloyd-Knight and J.G. Boal. 2007. UV radiation influences covering behaviour in the urchin Lytechinus variegatus. Journal of the Marine Biological Association of the United Kingdom. 87: 1257-1261.

Snellen, C.L., P.J. Hodum and E. Fernándes-Juricic. 2007. Assessing western gull predation on purple sea urchins in the rocky intertidal using optimal foraging theory. Canadian Journal of Zoology. 85: 221-231.

9 March 2011 Christina Ball Royal BC Museum Phil Lambert Telford, M. and R. Mooi. 1996. Podial particle picking in Cassidulus caribaearum (Echinodermata: Echinoidea) and the phylogeny of sea urchin feeding mechanisms. Biological Bulletin. 191:209-223.

Wilkie, I.C. 2002. Is muscle involved in the mechanical adaptability of echinoderm mutable collagenous tissue? The Journal of Experimental Biology. 205:159-165.

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