White Sea Urchin
(Linnaeus 1758)

salmacis urchin.jpg
Figure 1. Salmacis sphaeroides (Linnaeus, 1758). Image by Phua Jun Wei

Who wants to cuddle a sea urchin?


Cute and cuddly are words people happily associate with furry mammals, particularly if they were recently born. But isn’t the sea urchin in the picture above at least fairly adorable? Most people associate sea urchins either with venomous spines or their edible gonads (uni in Japanese), but I like to think Salmacis sphaeroides, with its awkward dome shape and a penchant for dressing itself up, is very cute indeed. And yes it can be cuddled, as long as you take care to not damage its spines, which are incapable of drawing blood (unless you throw it at someone, and with quite a bit of force too).

This sea urchin is common to many of Singapore’s shores(1) , so it lives right beside many of us, playing an important role in the tropical seagrass community(2) . The layperson would likely not be familiar with it, because they are only easily found in intertidal habitats. There is also much to be discovered about its ecology. This webpage targets both the aspiring naturalist and the scientific research community, so read on if you belong to the first, and use the hyperlinks to skip to relevant sections if you belong to the second!

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Figure 2. Cute and cuddly urchins. Image by Phua Jun Wei

Habitat & Distribution


Salmacis sphaeroides prefers muddy sublittoral (below the intertidal area) habitats, but they are commonly found in the intertidally in silty, almost muddy soft sediments(3). They are often associated with macroalgae (seaweeds) and seagrass meadows. Sometimes they are found in large numbers on intertidal walks, which might be associated with mating behaviour(4). (see the section on Reproduction if you want to know why!)

Globally, this tropical species is found in the Indo-West Pacific, ranging from China down to Australia(5). Locally, it is often sighted on the northern shores, especially Changi Beach(1). It has also been spotted in some of the southern islands. Below is a map showing where it has been found in local waters:



Field Identification


It takes some time to be able to spot this urchin! This is because it tends to cover itself with all sorts of things, but especially shells, shell debris and seaweed. It is easier to keep an eye out for lumps of material that look as if they have been gathered together. Once you have found an individual (usually between 5-10cm)(6), it is easiest to identify them by their greenish-white tests (their shells) and maroon bands on their spines. There might be some variation in the banding. For a detailed anatomical diagnosis, see the sections on Taxonomy and Diagnosis.

Here’s a table showing the differences amongst S. sphaeroides and its rarer relatives:
Species
Spines
wildsingapore salmacissphaeroides1.jpg
wildsingapore salmacissphaeroides2.jpg
Salmacis sphaeroides. Test is
typically greenish-white.
Spines have maroon bands that can be
dispersed throughout their entire lengths.
The bands may be light or dark, and can
also be green.
wildsingapore salmacisvirgulata1.jpg
wildsingapore salmacisvirgulata2.jpg
Salmacis virgulata. Test is also
greenish-white.
There is only one solid maroon band
towards the tip of each spine.
wildsingapore salmacisbicolor1.jpg
wildsingapore salmacisbicolor2.jpg
Salmacis bicolor. Test is white but
appears red because the base of each
spine is red.
Spines are red at the base, and continue
with white and maroon bands.
Table 1. The three species in Singapore belonging to the genus Salmacis.
Images taken from www.wildsingapore.com/wildfacts/ and owned by Ria Tan.

Diet


Sea urchins eat with an organ known as the Aristotle’s lantern, which looks like the claw on those arcade machines that is used to grab at stuffed toys, except with more teeth (five to be exact). These teeth work in unison, rasping against surfaces to remove edible material. Various experiments have confirmed that S. sphaeroides is a generalist, feeding on a variety of seagrasses(2) and macroalgae(7), two other species of sea urchins, sea pens, jellyfish, and a rather random plethora of experimentally introduced food items, such as banana skins and salami(8)! They have also been observed attacking and preying on members of their own species(8).


Video 1: Movement of the Aristotle's lantern during feeding. Note that this is not S. sphaeroides,
Obtained from YouTube under fair use.

Behaviour


Sensing with podia

The sea urchin’s tube feet are incredible things. They are responsible for locomotion, respiration(9) and even photoreception! There may be slight differences in the length, thickness and proteins of different podia, because they serve different functions. The podia on the oral surface, for example, are mostly use for walking(9). Podia also contain opsins (light-sensing proteins) and express genes related to photoreception (such as PAX6)(10). They thus play a role in the well-documented shadow reaction, which involves the waving of spines when a shadow is cast over the urchin(11).
IMG_3807.JPG
IMG_3710.JPG

Figure 3. Podia are the translucent tubes that the urchin is using to attach itself onto the styrofoam. Podia separated from the urchin are shown on the right. Image by Phua Jun Wei.



Covering response: some hypotheses

Salmacis sphaeroides individuals are often found with plenty of items covering its aboral surface. They pick these up with their podia (tube feet), which can work like a conveyor belt to move them around. No one knows for sure why they (and many other species of sea urchins) do this, but several hypotheses have been proposed, which probably are relevant in varying degrees for different species(12). In general, smaller sea urchins seem to cover themselves more for any of the hypotheses that involve protection(12)(13), which might represent an energetic trade-off with foraging.

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Figure 4. Salmacis sphaeroides covering itself with various items.
Image by Tan Yong Guang.

1. Protection from ultraviolet radiation

UV radiation is dangerous to many marine organisms because it destroys DNA. It has been shown experimentally that urchins have greater mortality when subjected to UV radiation(14)(15). Picking up opaque materials might help shade the urchin from this(16). One experiment in 1975 even showed that another species of urchin moved stones around to track a beam of light, and numerous others have demonstrated that it is UV radiation that induces a greater covering response, as opposed to just visible light(18)(19). Many sea urchins are also negatively phototaxic(18); they avoid sunlight by moving to shaded areas. The amount of pigmentation on the urchin’s test may also be related to the degree to which they cover themselves(20), because it affords protection from UV radiation, much like darker skin. Given that S. sphaeroides is largely white in colour, it is possible that this species might be even more susceptible to UV radiation than other species.

2. Protection from wave action

Waves can dislodge urchins and cause them to be flung onto hard surfaces, damaging their spines, which are costly to repair(12). Waves can also cause floating debris to slam into urchins with greater force. Thus, sea urchins might cover themselves during periods of strong wave action(12)(21). The covering materials might serve to increase their mass, preventing dislodgement, or protect their spines from damage.

We conducted an experiment to test the hypothesis that wave action would trigger the covering response in S. sphaeroides. Urchins were placed in tubs of seawater, which were either left on the shore or rocked by the waves. As expected, the urchins exposed to wave action covered themselves more. We also saw that the shells were positioned on the lateral aspect of their aboral surface, which is a similar observation in other papers(12)(21). This might help to streamline the urchins, thus stabilising them.
external image 18ORfh5Zc7nff72ZypTaSiKxo5Mo-eABLxmJxW7JdeBnVAIbND2ptidj0yi3zkJlyzlAyjrcYE3oiHQQmGpdsoA1N1nounxXs3QO8-sicr8IzjWcMYkDSRBMx1QevL9Ffon6EGFB7g
Figure 5. Salmacis sphaeroides covering itself laterally after being subjected to wave action.
Image by Darren Lee.
However, we also noted that the urchins tended to have many of their podia extended omni-directionally, perhaps because these are also involved in other functions, as mentioned before. Perhaps this represents an additional mode of material acquisition, especially when wave action is present, as actively searching for items may be dangerous under such conditions(12); a study has shown that (another species of) sea urchin decreases its foraging activity in the presence of strong waves(22).

IMG_3808.JPG
Figure 6. Salmacis sphaeroides with podia extended omni-directionally.
Image by Phua Jun Wei.

3. Camouflage

Various studies have investigated the covering behaviour of different species of sea urchins when exposed to predators and have arrived at different conclusions(12)(13)(23). It is reasonable to hypothesise that S. sphaeroides will be able to improve its chances of survival from predation by camouflaging itself. However, this would only be effective against visual predators, and likely have no effect on chemosensory predators.

4. Food Storage

Some scientists suggest that sea urchins carry a larder of food around, in order to deal with a supply shortage(24)(25). However, this hypothesis has little evidence and few experiments have been carried out to test it.

Defense from Predators

Other than the possible camouflage offered by its covering behaviour, S. sphaeroides has one other important adaptation to protect itself: the defense response by its numerous spines(26), which line the aboral surface.

The spines are controlled by catch connective tissue and muscles, which are in turn controlled by nerves(27). Catch connective tissue is present in echinoderms, and is responsible for the stiffening you might notice if you pick up a sea star or a sea cucumber. Together, the catch connective tissue and muscles change the position of the spines in response to different situations. If something touches the spine, it stiffens and points straight up, working like a spear to defend the test. On the other hand, if a predator touches the test, the spines in that area converge and flatten to form a defensive barrier(28).

Reproduction


Sexual reproduction is the overwhelming mode in sea urchins. Individuals are gonochoristic (separate sexes in each), with hermaphroditism being extremely rare(29), and S. sphaeroides probably has a breeding season(6), because individuals gather in large numbers, often in shallow waters, presumably to spawn. The close proximity helps increase the success of fertilisation(4), but the reason for spawning in shallow waters is a subject of controversy. This is because shallower waters often means increased water flow, which has been associated with sperm dilution and thus decreased fertilization(30). However, a recent study has pointed out that those results were associated with unidirectional flow, which does not characterise flow in shallow coastal waters(31). Instead, shallow waters are often subjected to turbulent, oscillatory flow, and the right amount may in fact increase the success of fertilization(31)(32).

An alternative argument is that shallow waters contain seagrass meadows, which help to slow down velocity and thus increase fertilisation success(33).

wildsingapore salmacisspawn.jpg
Figure 7. Salmacis sphaeroides occasionally gather in large numbers,
perhaps to spawn in shallow waters. Image taken from
www.wildsingapore.com/wildfacts/ and owned by Ria Tan.

Community Interactions


Predators

A variety of animals probably prey on this species, but information is lacking. Any contribution on information is welcome.

Commensal organisms

The most well-documented association S. sphaeroides has is with the commensal annelid worm, Oxydromus angustifrons, which tends to live in the peristomial groove just outside the ring of teeth on its oral surface. The worm probably does no harm to the urchin, and lives off tiny algae and plankton found on the urchin’s food sources. The urchin represents a microhabitat for the worm, and a positive correlation has been found between the size of the urchin and the number of worms living on it(34). So treasured is the urchin that the worms will aggressively defend their territory from other worms!


wilssingaporeworm.jpg
Figure 8. O. angustifrons in the peristomial groove on the
oral surface of S. sphaeroides.Image taken from
www.wildsingapore.com/wildfacts/ and owned by Ria Tan.

Importance


Ecologically, sea urchins in general are important grazers that affect the abundance of seagrass and macroalgae(2); this has sometimes led to the destruction of habitats when the natural predators of sea urchins are removed(35). The status of S. sphaeroides has never been assessed in Singapore.

The scientific community is interested in the developmental biology of sea urchins, because their larvae and embryos are transparent and easy to study.

There is considerable interest in the cultivation of S. sphaeroides(6), in order to relieve the pressure on sea urchin fisheries worldwide, as the demand for the edible gonads continue to grow.

It has also been explored as a biological anti-fouling agent due to its large appetite(7)!

Development


The following information is adapted from Rahman et al. (2012)(36). Please refer to the paper for a more complete version.

Following fertilization in the water column, the embryo develops into a blastula in about 9 hours. A series of larval stages follows, in which the larvae acquires more and more arms, and develops tube feet and spines within the larval body. Up to this point, the process takes about 35 days. Competent larvae swim near the surface of the substrate to determine a suitable site for settlement. After attachment, larval structures are either discarded or resorbed, and adult features continue to develop in the juvenile.

Taxonomy


Classification

The various species within the genus Salmacis have traditionally been difficult to delimit(37), with the latest revision done in 1943(38). Salmacis sphaeroides belongs to the family Temnopleuridae, order Camaradonta. The traditional taxonomical classification is given in the table below, referenced from the World Register of Marine Species(39).

Synonyms:
Echinus sphaeroides Linnaeus, 1758
Salmacis globator Agassiz, 1846
Salmacis sulcatus Agassiz, 1846
Melebosis mirabilis Girard, 1850
Salmacis pyramidata Troschel, 1866
Salmacis festivus Grube, 1868
Salmacis sulcata Agassiz, 1872

Subspecies:
Salmacis sphaeroides sphaeroides (Linnaeus, 1758)
Salmacis sphaeroides variegata Mortensen, 1942

taxon.jpg
Table 2. Classification of S. sphaeroides.

History of Species Name

According to Kroh (2011)(42), the current type specimen was originally classified as Melebosis mirabilis by Girard (1850)(40). This was classified as a junior synonym of Salmacis sulcata by Agassiz (1872)(41). I have not been able to trace the history further, as I am unable to obtain a copy of the monograph by Mortensen (1943)(38), but the type specimen must have been compared to the holotype (Echinus sphaeroides) described by Linnaeus in 1758, the latter of which may have been lost or degraded beyond recognition.

Diagnosis


The diagnosis of individual species of sea urchins is dependent on the morphology of the dried test. The following guide allows one to distinguish only up to the level of genus. It is adapted from the London Natural History Museum website(42). Detailed keys are available at this link. Please use Figure 9 as a reference for identifying regions on the aboral surface of the urchin. In particular, the ambulacral plates are crucial to the diagnosis.

overall pic.jpg
Figure 9. Aboral view of S. sphaeroides test. Abbreviations: P = periproct,
AD = apical disc, AZ = ambulacral zone, IZ = interambulacral zone, AS = adradial
suture, IS = interambulacral suture, PS = perradial suture. Image by Phua Jun Wei.
Recognising individuals from the Temnopleuridae is relatively easy because the ambulacral plating is of the compound echinoid style (Figure 10a), and there are sharp-edged pits along the sutures (Figure 10b).
compound echinid style ambulacral plate.jpg
sutural pits.jpg
Figure 10a. The irregular shapes mark out a single compound ambulacralplate. Note how the three components of the compound plate divide theprimary tubercle (largest tubercle within the shapes) - this is the compound echinid style. Note also that each component contains two holes adradially - this is known as a pore pair. This ambulacral plate is thus trigeminate (three pore pairs). AZ = ambulacral zone. Image by Phua Jun Wei.
Figure 10b. The zig-zag line is the interradial suture. Note the pits at each junction (where three plates meet). With greater magnification it will be evident that the pits are sharp-edged. Image by Phua Jun Wei.
The genus Salmacis has the following characteristics, which may be shared with other genera in the Temnopleuridae: There is no sexual dimorphism in the test, the periapical region is not sunken as a marsupium (pouch) (Figure 11a), the interambulacral plate is twice as wide as it is tall (Figure 11b), the apical disc is smaller than the peristome (Figure 11c/d). Pits are punctiform, with pore pairs in offset triads (Figure 10a). There are no naked areas in the interradial and perradial zones, i.e. they are studded with tubercles throughout their entire length (Figure 11b/e). The primary tubercles (on ambulacral plates) are large and distinctly crenulate (Figure 11f).

The next two characteristics are unique to the genus Salmacis, and can be used to distinguish it from the closely related genus Salmaciella. These are: the presence of a primary tubercle on every ambulacral plate, as opposed to every other ambulacral plate (Figure 11f), and each plate has a larger adradial primary tubercle and a smaller perradial secondary tubercle (Figure 11f).

periapical region.jpg
interambulacral plate twice wide as tall.jpg
Figure 11a. The periapical region is demarcated by the ellipse. It is not sunken into a pouch. Image by Phua Jun Wei.
Figure 11b. The interambulacral plate has a width that is more than twice its height. Also, the interradial zone (the areas immediately adjacent to the interradial suture) is studded with tubercles. IZ = interambulacral zone, IP = interambulacral plate. Image by Phua Jun Wei.
apical disc diameter.jpg
peristome diameter.jpg
Figure 11c. The apical disc diameter is marked out as shown.
Image by Phua Jun Wei.
Figure 11d. The peristome diameter is marked out as shown, and is larger than the apical disc diameter. Image by Phua Jun Wei.
nonnaked perradial zone.jpg
last picture.jpg
Figure 11e. The perradial zone (the areas immediately adjacent to the perradial suture) is studded with tubercles . AZ = ambulacral zone. Image by Phua Jun Wei.
Figure 11f. This is the ambulacral zone. Primary tubercles are on the adradial side of every ambulacral compound plate, and are larger than the secondary tubercles, which are on the perradial side. PT = primary tubercle, ST = secondary tubercle, C = crenulations. These two features distinguish the genus Salmacis from the genus Salmaciella. Image by Phua Jun Wei.

Phylogeny


The clade Temnopleuridae was previously found to be paraphyletic by Smith (1988)(43), but shown to be monophyletic by Jeffery et al. (2003)(37). A later paper by Kroh and Smith (2010) , the latter of whom authored the 1988 paper, seemed to agree on this. Relationships within the family continue to be unresolved (Figure 12), with two subgenera (Temnopleurus and Toreumatica) shown to be less related to each other than to other genera(37). Other genera are also paraphyletic. However, various analyses derived the same relationship between the genera Salmacis, Salmaciella and Temnopleurus (Temnopleurus)(37)(45). The order Camaradonta, to which the Temnopleuridae belong, is a monophyly, but may be wrongly rooted in the tree due to the lack of molecular data from the Parasalenidae (Figure 13)(44).

jeffery 2003 temnopleurid phylogeny correct.jpg
Figure 12. Proposed phylogeny of Temnopleuridae. Representative
species from the various genera within the clade are indicated by the red line.
It is apparent that various genera are not monophyletic. Numbers beside
nodes indicate bootstrap values. Image modified from Jeffery et al. (2003),
pending permission from the publishers.

temnopleurids.jpg
Figure 13. Proposed phylogeny of Camaradonta. The authors suspect it is wrongly rooted due to the
lack of molecular data for Parasalenidae, represented by the genus Parasalenia. The sole representative
for Temnopleuridae is the genus Temnopleurus. Bootstrap values are indicated beside the nodes, and are
extremely low due to the massive number of taxa (169 across all post-Palaeozoic echinoids). Image
modified from Kroh & Smith (2010), pending permission from the publishers.

References


1. "White salmacis urchin," by Tan, R. Wild Singapore, Jan 2014. URL: http://www.wildsingapore.com/wildfacts/echinodermata/echinoidea/urchin/sphaeroides.htm (Accessed 10 Oct.2015).

2. Klumpp, D. W., J. T. Salita-Espinosa & M. D. Fortes, 1993. Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquatic Botany, 45(2-3): 205-229.

3. Tan, L. W. H. & P. K. L. Ng, 1992. A guide to seashore life. Revised Edition. Singapore Science Centre, Singapore. 160 pp.

4. Lauzon-Guayl, J.-S. & R. E. Scheibling, 2007. Importance of spatial population characteristics on the fertilization rates of sea urchins. The Biological Bulletin, 212(3): 195-205.

5. Lane, D. J. W., L. M. Marsh, D. Vanden-Spiegel & F. W. E. Rowe, 2000. Echinoderm fauna of the South China Sea: An inventory and analysis of distribution patterns. Raffles Bulletin of Zoology, Supplement 8: 459-493.

6. Rahman M. A., F. M. Yusoff, A. Arshad, S. M. N. Amin & M. N. Shamsudin, 2013. Population characteristics and fecundity estimates of short-spined white sea urchin, Salmacis sphaeroides (Linnaeus, 1758) from the coastal waters of Johor, Malaysia. Asian Journal of Animal and Veterinary Advances, 8(2): 301–308.

7. Ng, C. S. L., T. C. Toh, K. B. Toh, J. Guest & L. M. Chou, 2014. Dietary habits of grazers influence their suitability as biological controls of fouling macroalgae in ex situ mariculture. Aquaculture Research, 45(11): 1852-1860.

8. Tsuchiya M., M. Nishihira, S. Poung-In & S. Choohabandit, 2009. Feeding behavior of the urchin-eating urchin Salmacis sphaeroides. Galaxea, Journal of Coral Reef Studies, 11: 149–153.

9. Leddy, H. A., A. S. Johnson, 2000. Walking versus breathing: mechanical differentiation of sea urchin podia corresponds to functional specialization. The Biological Bulletin, 198(1): 88-93.

10. Lesser M. P., K. L. Carleton, S. A. Bottger, T. M. Barry, C. W. Walker, 2011. Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. Proceedings of the Royal Society of London B: Biological Sciences, 278(1723): 3371–3379.

11. Milliott N. & M. Yoshida, 1960. The shadow reaction of Diadema antillarum Philippi. Journal of Experimental Biology, 37:363-375.

12. Dumont, C.P., D. Drolet, I. Deschenes& J.H. Himmelman, 2007. Multiple factors explain the covering behaviour in the green sea urchin, Strongylocentrotus droebachiensis. Animal Behaviour, 73(6):979–986.

13. Scheibling, R. E. & J. Hamm, 1991. Interactions between sea urchins (Strongylocentrotus droebachiensis) and their predators in field and laboratory experiments. Marine Biology, 110(1): 105-116.

14. Lees, D. C. & G. A. Carter, 1972. The covering response to surge, sunlight, and ultraviolet light in Lytechinus anamesus (Echinoidea). Ecology, 53(6): 1127–1133.

15. Belleza D. F. C., R. S. A. J. Abao, C. A. Taguba & D. T. Dy, 2012. Effects of UV-C on the masking behaviour of the green urchin Salmacis sphaeroides (Linnaeus, 1758). The Philippine Scientist, 49: 34–43.

16. Amato K. R., S. L. Emel, C. A. Lindgren, K. M. Sullan, P. R. Wright & J. J. Gilbert, 2008. Covering behavior of two co-occurring Jamaican sea urchins: differences in the amount of covering and selection of covering material. Bulletin of Marine Science, 82(2): 255–261.

17. Millott, N., 1975. The photosensitivity of echinoids. Advances in Marine Biology, 13: 1–52.

18. Adams, N.L., 2001. UV radiation evokes negative phototaxis and covering behavior in the sea urchin Strongylocentrotus droebachiensis. Marine Ecology Progress Series, 213:87–95.

19. Verling, E., A. C. Crook& D. K. A. Barnes, 2002. Covering behaviour in Paracentrotus lividus: is light important? Marine Biology, 140(2): 391–396.

20. Kehas, A. J., K. A. Theoharides & J. J. Gilbert, 2005. Effect of sunlight intensity and albinism on the covering response of the Caribbean sea urchin Tripneustes ventricosus. Marine Biology, 146(6): 1111–1117.

21. James, D. W., 2000. Diet, movement, and covering behaviour of the sea urchin Toxopneustes roseus in rhodolith beds in the Gulf of California, Mexico. Marine Biology, 137(5): 913–923.

22. Gagnon, P., P. St-Hilaire-Gravel, J. H. Himmelman & L. E. Johnson, 2006. Organismal defenses versus environmentally-mediated protection from herbivores: unraveling the puzzling case of Desmarestia viridis (Phaeophyta). Journal of Experimental Marine Biology and Ecology, 334(1): 10–19.

23. Agatsuma, Y., 2001. Effect of the covering behavior of the juvenile sea urchin Strongylocentrotus intermedius on predation by the spider crab Pugettia quadridens. Fisheries Science, 67: 1181-1183.

24. Dix, T. G., 1970. Covering response of the echinoid Evechinus chloroticus (Val.). Pacific Science, 24(2):187–194 .

25. Douglas, C. A., 1976. Availability of drift materials and the covering response of the sea urchin Strongylocentrotus purpuratus (Stimpson). Pacific Science, 30(1): 83–89.

26. Strathmann, R. R., 1981. The role of spines in preventing structural damage to echinoid tests. Paleobiology, 7(3): 401-406.

27. Motokawa, T. & Y. Fuchigami, 2015. Coordination between catch connective tissue and muscles through nerves in the spine joint of the sea urchin Diadema setosum. Journal of Experimental Biology, 218(5): 703-710.

28. Yoshida, M., 1962. The effect of light on the shadow reaction of the sea urchin, Diadema setosum (LESKE). Journal of Experimental Biology, 39(4): 589-602.

29. Boolootian, R. A. & A. R. Moore, 1956. Hermaphroditism in echinoids. The Biological Bulletin, 111(3): 328-335.

30. Levitan, D. R., M. A. Sewell & F. -S. Chia, 1992. How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology, 73(1): 248-254.

31. Kregting, L. T., A. L. Bass, O. Guadayol, P. O. Yund & F. I. M. Thomas, 2013. Effects of oscillatory flow on fertilization in the green sea urchin Strongylocentrotus droebachiensis. Public Library of Science One, 8(9): e76082.

32. Crimaldi, J. P. & H. S. Browning, 2004. A proposed mechanism for turbulent enhancement of broadcast efficiency. Journal of Marine Systems, 49(1-4): 3-18.

33. Simon, T. N. & D. R. Levitan, 2011. Measuring fertilization success of broadcast-spawning marine invertebrates within seagrass meadows. The Biological Bulletin, 220(1): 32-38.

34. Chim, C. K. & J. L. L. Ong, 2013. An association between a hesionid polychaete and temnopleurid echinoids from Singapore. Cahiers de Biologie Marine, 54: 577-585.

35. Duggins, D. O., 1980. Kelp beds and sea otters: an experimental approach. Ecology, 61(3): 447-453.

36. Rahman, M. A., F. M. Yusoff, A. Arshad, M. N. Shamsudin & S. M. N. Amin, 2012. Embryonic, larval and early juvenile development of the tropical sea urchin, Salmacis sphaeroides (Echinodermata: Echinoidea). Scientific World Journal, 2012: e938482.

37. Jeffery, C. H., R. B. Emlet & D. T. Littlewood, 2003. Phylogeny and evolution of developmental mode in temnopleurid echinoids. Molecular Phylogenetics and Evolution, 28(1): 99-118.

38. Mortensen, T., 1943. A Monograph of the Echinoidea. III, 2. Camarodonta. I. Orthopsidae, Glyphocyphidae, Temnopleuridae and Toxopneustidae. C. A. Reitzel, Copenhagen, vii+553 pp.

39. "Salmacis sphaeroides (Linnaeus, 1758)," by Kroh A., World Echinoidea Database, 2015. URL: http://www.marinespecies.org/echinoidea/aphia.php?p=taxdetails&id=513533 (Accessed 5 Nov 2015).

40. Boston Society of Natural History, 1851. Proceedings of the Boston Society of Natural History. Bolles and Houghton, Cambridge, 396pp.

41. Agassiz, A., 1872. Revision of the Echini: Illustrated catalogue of the museum of comparative zoölogy at Harvard College, no. 7. Cambridge University Press, Cambridge, 762pp.

42. "The Echinoid Directory," by Smith, A. B. & A. Kroh (editors), Natural History Museum, 2011. URL:http://www.nhm.ac.uk/research-curation/projects/echinoid-directory (Accessed 27 Oct 2015).

43. Smith, A. B., 1988. Phylogenetic relationship, divergence times, and rates of molecular evolution for Camarodont sea urchins. Molecular Biology and Evolution, 5(4): 345-365.

44. Kroh, A. & A. B. Smith, 2010. The phylogeny and classification of post-Palaeozoic echinoids. Journal of Systematic Palaeontology, 8(2): 147-212.

45. Janies, D. A., J. R. Voight & M. Daly, 2011. Echinoderm phylogeny including Xyloplax, a progenetic asteroid. Systematic Biology, 60(4): 420-438.