Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Cali. B iol. Mar. (2013) 54 : 729-734 Why do brittle stars emit light? Behavioural and evolutionary approaches of bioluminescence Alice JONES and Jérôm e M ALLEFET M arine biology laboratory, Catholic University o f Louvain, 3 Place Croix du Sud, B ox L 7 .06.04, B -134S Louvain-la-Nettve, Belgium. Fax: + 32 (0)10 47 34 76, E-fnail: alice.jones(cb.uclouvain.be A b s tra c t: In this study, we investigated the functions o f biolum inescence (the production o f light b y living organism s) in five brittle star species. Bioliuninescence is a w idespread phenom enon in the marine environm ent, and is especially abundant in the class Ophiuroidea. It is assum ed that light in marine invertebrates m ainly plays a role o f defense against predation, and many m echanism s o f defense have been proposed for brittle stars. We investigated the potential functions o f startle effect (use o f light to deter predator), use o f light to advertise a predator that the prey is toxic (aposem atic signal) and attraction o f a secondary predator (function usually called “burglar-alarm effect”). Predatory experim ents, involving one or tw o predators trom different trophic levels allow ed us determ ining benefits o f the light em ission fo r several brittle star species. We clearly dem onstrated that the three functions cited behind are used in brittle stars. It is clear now that brittle stars use a w ide variety o f defensive m echanism s involving light. R é su m é : Pourquoi les ophiures émettent-elles de la lumière ? Approches com portem entales et évolutionnistes de la hiolum inescence. Cette étude porte sur les fonctions de la biolum inescence (la prodùction de lum ière p ar des organism es vivants) chez cinq espèces d ’ophiures. La biolum inescence est mi phénom ène courant dans le m ilieu m arin, et il est particulièrem ent abondant dans la classe des ophiuridés. Il est adm is que la biolum inescence joue un rôle de défense contre la prédation chez les invertébrés benthiques. Plusieurs m écanism es de défense ont été suggérés pour les ophiures. Nous avons investigues les fonctions potentielles de “startle effect” (répulsion du prédateur par la lum ière), d ’utilisation de la lum ière pour prévenir le prédateur que sa proie est toxique (signal aposém atique) et d ’attraction d ’un prédateur secondaire (fonction com m uném ent appelée “burglar-alarm ” ) ont été testées. Des expériences de prédation, faisant intervenir des prédateurs d ’u n ou deux niveaux trophiques, nous ont perm is de situer les bénéfices associés à ré m issio n de lum ière pour plusieurs espèces d’ophiures. Les trois fonctions citées plus haut ont pu être clairem ent dém ontrées chez les ophiures. II est m aintenant clair que les ophiures utilisent une grande variété de m écanism es de défense im pliquant la lum ière. Keyw ords: Biolum inescence • Ophiuroid • À posem atism • Burglar-alarm • Ethology Introduction Biolum inesccnce, the emission o f visible light by living organism s (for a review see Haddock et al., 2010), is a com m on feature in echinoderm s, especially in brittle stars. in this class, at least 77 luminous species are known (M allefet, 2012), o f 222 species tested, with a total o f 2,128 species and subspecies described (Stöhr 8c O ’Hara, 2012). This abundance o f lum inous species, discovered recently (M allefet, 2012) suggests th at lig h t production has im portant functions in these organism s. Functions o f biolum inescence can be divided in three categories: intraspecific com m unication, help w ith predation, and defense against predation. Studies suggest that the function 730 FU N C T IO N OF O PH IU RO ÏD L U M IN ESC EN C E o f biolum inescence in brittle stars involve defense against predation (H erring, 1.995), such as startle effect (deterrence o f predators by intense flashes), sacrificial lure (autotomy o f a lum inous distal part o f arm s w hen attacked), aposem atism (use o f a conspicuous signal to advertise predators that the prey is toxic or unpalatable), or burglar alarm effect (use o f light to attract secondary predator). We investigated the biolurninescence functions in five lum inous ophiuroids w ith prey -p red ato r experim ents: A m phiura arcystata (H .L. Clark, 1911), A m phipholis squam ata (D elle C hiaje, 1828), O phiocom ina nigra (Abildgaard, in O.F. Müller, 1789), Ophiopsila aranea (Forbes, 1843) and O phiopsila californica (A.H, Clark, 1921). These species differ in their lum inous pattern and colour. W hile O. aranea and 0 . californica are known to emit intense green flashes, the lum inous signal o f A. squam ata is far lower. O phiocom ina nigra emits very weak luminous m ucus w hen disturbed (Fontaine, 1964). The last species, A, arcystata, em its a blue light. Finally, a sixth species, O phiothrix fra g ilis (A bildgaard, in. O.F. Müller, 1789) w as used as non biolum inescent control. As predator, we chose the crab Carcinus m aenas (Linnaeus, 1758). This species is comm on in both the North Sea and in the M editerranean Sea. M oreover, this species was interesting because it is known to prey on echinoderms (M untz el al„ 1965). Crabs w ere used sighted or blinded, to com pare behaviour betw een crabs able or unable to see biolum inescence. A secondary predator, the fish Diplodus vulgaris (G eoffroy Saint-Hilairc, 1817), com mon in the M editerran ean Sea, w as u sed for burglar alarm experim ents, because it preys on crabs (pers. Obs.). M any experim ents are conceivable to asses i f . biolum inescence is involved in defensive functions in ophiuroids. If light is used to deter predator, bioluminescent prey should suffer lower predation than non bioiuminescent ones w hen bioluminescence is visible, m eaning during the night and w ith sighted crabs. I f light- is used to advertise predators that the ophiuroid is toxic or unpalatable (aposematic signal), it means that, on one hand, ophiuroids arc unpalatable and, on the other hand, predator are able to associated the ophiuroid unpalatability with its luminous signal. Finally, if light is used to attract a secondary predator, it means that the prim ary predator (the crab) should be more predated by t,he secondary predator (the fish) when a luminous ophiuroid is present. It means also that the ophi uroid should be less predated when the fish is present. O ur experim ents on ophiuroids can then be listed as a set o f questions: • Does ophiuroid biolum inescence deter predators? • Does ophiuroid biolum inescence advertise predators? (i) A re ophiuroids unpalatable? (ii) A re predators able to associate unpalatability and lum inous signal? • Does ophiuroid bioluminescence attract a secondary predator? Material and M ethods Sam pling Brittle stars were collected between 2007 and 2012 in France and in California. Ophiopsila aranea was collected at ARAGO marine station at B anyuls-sur-m er (France) using SCUBA, and 0 . nigra and A. squam ata w ere collected in N orth France, Wimeretix, by trawl and directly on the shore, respectively. The non-biolum inesccnt control species O, fragilis was also collected in W im ereux by trawl. Ophiopsila californica and A, arcystata were collected in Santa B arbara cam pus, U niversity o f C alifo rnia, by SCUBA. Predators, crabs Carcinus m aenas and the fish D iplodus vulgaris were collected in W im ereux and Banyuls, respectively. D oes ophiuroid bioluminescence deter predators? To determine the potential deterrent effect o f light for predators, experiments were run on the five lum inous brittle star species. Crabs C. m aenas w ere u se d as predators. For each test a brittle star and a crab w ere put in contact in an aquarium o f 601, with a stone in tile center to provide shelter. Each experiment lasts 12 hours, and was repeated six times during the day, and six tim es during the night with each species. The ophiuroids w ere w eighed before and after to estimate the amount o f tissue lost during the experiment. This index (weight o f brittle star eaten) was, standardized by the weight o f the predator and called “predation rate”; Experiments were repeated during a day/night cycle, to highlight a possible influence o f the bioluminescence on the predatory behaviour o f the crabs in the dark, w hen it is the m ost clearly seen. We also ran this experim ent with blinded crabs. Experim ents were repeated w ith blinded crabs six times during the day and six tim es during the night. Crabs were blinded by painting the distal part o f the eyestalk black, with nail polish, as used in other studies (for example see Duffy et al., 2006). D oes ophiuroid bioluminescence advertise predators? (i) Are ophiuroids unpalatable? A posem atism is the use o f light or bright colors to warn a predator that the prey is toxic or unpalatable. Since association betw een a conspicuous signal and unpalatabili ty is required for this to work, w e investigated the palatability o f the brittle star species. Tissues (arm s) o f the ophiuroids were mixed w ith agar to form blocks. B locks o f agar m ixed with fish pieces were also m ade, lo verify that agar itself has no deterrent effect since fish is the com m on 731 A. JONHS, J. M A LL EFE T crab diet in the laboratory. Each block was provided to a crab for 30 m in, in a small aquarium o f 10 I. Each block w as w eighed before and after the experiment, in order to evaluate the am ount o f agar eaten. This index, standardized b y the w eight o f the predator, was called consum ption rate. T he handling time o f the block by the crab, and the co n su m p tio n rate, w ere recorded as indicators o f palatability (the longer and the more the block is handled and consum ed, the more palatable is the species). D o es ophiuroid bioluminescence advertise predators? (¡i) Are predators able to associate unpalatability and lum inous signal? To study aposematism, we used the species O. nigra and the species O. fragilis as non bioluminescent control. Crabs were placed in contact repeatedly with the ophiuroid, to see if the crab w ould avoid the ophiuroid after the emission o f light, w h ich w ould suggest aposem atic use o f the bioluminescence. One brittle star and one crab were put on a sm all aquarium (10 1) during four successive trials o f 30 minutes. Betw een'tw o trials, the brittle star was removed for 20 m inutes. The consumption o f brittle star was recorded for each trial. Experiments were a m six times during the day and six times during the night with both ophiuroid species, to distinguish the effect o f the biolum inescence. Indeed, biolum inescence is visible for the crabs only at night. Experim ents w ere also run during the day to verify that no other deterrent mechanisms were involved in the avoidance learning. D o e s ophiu ro id biolum inescence attract a secondary p red a to r? Finally, w e studied burglar alarm effect on O. aranea (using O, fra g ilis as non-bioluminescent control species). We put in contact brittle stars and predators from two different trophic levels (crabs C. maenas as primary predator, and fish D. vulgaris as secondary one). D ifferent prey-predators com binations were tested to assess the predation on brittle stars by crabs, fishes and both predators together. Predation rate on crabs by the fishes, in the presence or absence o f lum inous brittle stars, was also tested. Predatory experiments took place in a 100 1 aquarium, during 12 hours. Each preypredator com bination was repeatedly tested six times during the day, and six times during the night, Statistica l analysis A ll analyses w ere performed in JMP 8 or 10, using analysis o f variance and multiple m ean com parison test (HSD Tukey). Significance was always tested with the probability o f 0.05 ( P < 0.05). Results Does ophiuroid biolum inescence deter predators? Figure 1 illustrates the general effect o f biolum inescence as a w ay o f defense against predation. C om parisons betw een luminous and non-lum inous species, as w ell as blinded and sighted crabs allow us to estim ate the efficiency o f light as a defense against predation on a day/night cycle. We observed that w ith sighted crabs, the predation rale is always significantly higher during the day than during the night, w ith luminous brittle star species. With the nonluminous species, we observed the opposite result, although w ithout significant differences. P redation rates significantly increase w ith the blind crabs during the night, w hich indicates that vision o f biolum inescence is efficient to reduce predation. O. aranea wt b nt ■F O. nigra O. californica A. arcystata A squamata Ö. fragilis b ■* B . ■P ■pp— 0 0.05 0.1 0 0.05 0.1 Predation rate F ig u re 1. Predation rates for blind or sighted crabs, during day and night. HSD Tuckey, differen t letters in d icate strongly different m eans, n —6 for each com bination. D oes ophiuroid biolum inescence advertise p red a to rs? (i) A re ophiuroids unpalatable? Figure 2 shows the consum ption rate o f agar blocks made w ith different brittle star species. C onsum ption significantly differs according to the species (F K47 = 20.195, p < 0.001). Lower consum ption rate are observed in four species: O. aranea, O. californica, O. nigra after m echanical stress an d ri, arcystata. FU N C T IO N OF O PH IU R O ID LU M IN ESC EN C E 732 0,1 D oes ophiuroid biolum inescence a ttra ct a secondary predator? 0.09 o.os ab 0.07 0.0Û 0,05 0.04 003 0.Q2 i n Q .O i 0 . aranea ö. . californita O .níB ft 0 . nigra A. A .arcystata Oíraglllí dfstwrbad squam ata Fish F ig u re 2. C onsum ption rates o f agar blocks. HSD Tuckcy, different letters indicate strongly different m eans, n = 6 for each com bination. Figure 4A. shows predation rate on crabs, fo r different prey-predator combination: crab-fish; crab-fishriiiininous brittle star and crab-fish-non luminous brittle star, for experiments in day and night period. D uring the day, crabs are more predated for combinations including a brittle star. No significant differences appear betw een com bination with the luminous or the non-luminous ophiuroid. D uring the night, predation on crabs increases significantly in the combination with the luminous brittle star, but hot w ith the non-lum inous species. Results for predation suffered by brittle stars (Fig. 4B) show no significant differences betw een com binations (brittle star-crabs; brittle star-fish; brittle star-crab-fish) neither during the day nor during the night. D oes ophiuroid biolum inescence advertise predators? M (ii) A re predators able to associate unpalatability and lum inous sig n a l? D uring successive trials, it appears that the predation rate is higher for O, fra g ilis than for O. nigra, w hatever the trial or the p eriod (experim ent ran d uring day or night) (F | Q4 = 10.267, p = 0.002). M ultiple mean comparisons test shows that strong differences betw een predation in the successive trials appear in two com binations: with the species O. nigra during the night, and w ith the species O. fra g ilis during the day. F or O. nigra during the night, the consum ption o f brittle star is significantly higher during the first trial than during the tw o last trials, where the consum ption is null. For the com bination 0 . fragilis!day, predation rate is higher fór the third trial. N o differences betw een trials appear for O, nigra diuing the day or for 0 . fra g ilis during the night (Fig. 3). C.M o w w í ù. VJtQBfitlï’*predator) &tjrpnW(iümm9vs0f«y) -X" luminoyjpfcy) OT *vr im tt- N M 'X V- »«f * * g * F ig u r e 4. A. P red atio n on the prim ary, p re d a to r (crab C a m e n a s). HSD Tuckey, different letters indicate strongly different means n - 6 for each com bination). B. Predation on the brittle stars (ophiuroid O, aranea). HSD Tuckey, different letters indicate strongly different m eans n - 6 for each com bination. Discussion Does ophiuroid bioluminescence deter predators? È J1±2 1 4 Day 0, n ig ra Q .fragtils F ig u re 3. Predation rates during successive trials. HSD Tuckey, different letters indicate strongly different m eans, n = 6 for each com bination. Predation experim ents were u n dertaken to address questions o f the function o f the biolum inescence in ophiuroids. Brittle stars are vulnerable to predation at night with sighted crabs. This is uncom m on since crabs are com m only nocturnal predators. In contrast, this difference in predation rate and consumption disappears w ith blinded crab. Hence the predation experiments strongly suggest that the five luminous species exhibit a visual signal o f defense against their predators. The biolum inescence is thus most likely involved in the defense against predation in these species. D uring the day, there was no difference in predation o f luminous brittle stars and the control species A. JO N ES, J. M A LL EFE T O. fra g ilis, In addition, predation by blinded crabs does not differ betw een day and night. These results indicate that defense against predation in these ophiuroids are based on vision. N o other anti-predatory strategies such as chemical defenses seem sufficient to deter predators w ithout the biolum inescence. D o e s ophiuroid bioluminescence advertise predators? (i) A re ophiuroids unpalatable? T he palatability tests delivered interesting and surprising results. The palatability o f O. aranea, A, arcystata and 0. californica w as low. Concerning 0 . nigra, the palatability is strongly m odified by the release o f m ucus w hich has a strong deten*ent effect on the crabs. In absence o f the released m ucus, the tissue o f 0 , nigra is eaten as m uch as tissue o f 0 . fra g ilis or fish. We can conclude that the m echanical stress induces the release o f mucus, and that this mucus, includes both a visual w ay o f defense, the biolum inescence, and a deterrent com ponent These data su p p o rt the hypothesis o f the aposem atic use o f biolum inescence. A posem atic use o f biolum inescence has already been demonstrated for firefly larvae (De Cock & M atthysen, 2001 & 2ÖÖ3), for millipedes (M arek et ah, 2011) and in the brittle star species Ophiopsila aranea (Jones & Mallefet, 2010) and Ophiopsila riseii Llitken, 1859 (Grober, 1988), however controversy rem ains for this study (G uilford & Cuthill, 1989; Grober, 1989). The two brittle star species emit green intense flashes, a very d iffe re n t lum inous pattern than O. n ig ra , but the Lam pyridae larvae and millipeds (M arek et aL, 2011) emit slow glow ing light, which gets closer to the pattern o f O, n ig ra (D e C ock Sc M atthysen, 2001). E volution o f aposem atic signals requires precise conditions concerning appearance o f the signal as well as its m aintenance (Leimar et al., 1986). O nly low value prey (i.e. toxic or unpalatable prey) can evolve aposematic display. Regarding these palatability tests, this seems to be the case with m echanical ly stim ulated O. nigra,'Secondly, aposematic prey should suffer a low er predation rate than cryptic species. Predation experim ents show ed that also this condition is fulfilled for O. n ig ra . Finally, aposematic displays should allow the avoidance learning, o f the predator. D o es ophiuroid bioluminescence advertise predators? (ii) A re predators able to associate unpalatability and lum inous signal? W hen a crab is repeatedly in contact with O. nigra, during tile night, its consum ption o f brittle star significantly decreases along the trials. It seems that the crab actually avoids the prey, after two trials o f 30 minutes. In contrast, this difference does not appear during the day, w hen biolum inescence is not visible. The consumption does not 733 decrease w ith the control brittle star O, fra g ilis, w hich proves that the decrease in the first case cannot be explained by the satiety o f the crab. Avoidance learning also occurs with Ophiopsila aranea and O phiopsila riseii, but after only one trial (Grober, 1988; Jones & M allefet, 2010), which suggests that their strong signal m ay be m ore effective. The use o f selective light signals as aposem atic signals includes undeniable advantages. Actually, the light is em itted only after disturbance, for O. aranea and O. riseii as well as for O. nigra. The prey rem ains cryptic w hen not disturbed, and does not suffer the costs o f an increased detectability by naïve predators, which is a w ell-know n problem in the explanation o f the evolution o f aposem atic display (Eisner 8c Grant, 1981; G uilford & D aw kins, 1993; Speed 8c Ruxton, 2005). Thus O. nigra has an im portant advantage over the two other species.-Actually, the signal and the deterrent com ponent are both present in the sticky m ucus excreted outside the body w hen attacked. Here O. nigra takes advantage o f its defensive m echanism deterring its predator at the earlier stage o f their interaction. The em ission o f luminous mucus, after disturbance, seem s to be an advantageous strategy for aposem atic displays. H ow ever patterns differ strongly am ong brittle stars w ith luminous emission, aposematic use o f light seem s to include many evolutionary advantages, and this function of biolum inescence may have been underestim ated in the past, Further investigations, with other brittle star species, w ould allow generalizing the function o f light for these organisms and tackling the question o f the light function conservation in this class o f echinodertns. D oes ophiuroid biolum inescence a ttra ct a secondary predator? O ur observations concerning interactions betw een luminous brittle stars, crabs and fishes support the burglar alarm hypothesis. Indeed, during the night, the predation on crab by the fish is higher if O . aranea is present. This clearly indicates that light em itted by O. aranea can advertise the presence o f the crab to a predatory fish. D uring the day, w e observe thai predation rate on the crab increases when a brittle star is present, no m atter w hether the brittle star is lum inous or not. Since biolum inescence is not visible during the day, it sim ply indicates that hunting ophiuroids makes the crab less cryptic during the day hence m ore available for the fish. We also recorded predation rates on O. aranea. In this case, w e do not observe any difference betw een combinations. The predation rate on the brittle star is low er during night than day, but does not decrease w hen predators o f the two levels are present, contrary to w hat is predicted by the theory, i.e. lower predation rate on the luminous brittle star due to higher predation on the prim ary predator. These results support the use o f biolum inescence as 734 FU N C T IO N OF O PH IU RO ID L U M IN ESC EN C E burglar-alarm signal for 0 . a r a n e a , but w e suggest that the benefits o f this function m ight be visible at the level o f the population not for the single individual. Studies o f the genetic structure o f the Banyuls 0 . aranea population should in the future allow us to determ ine if a kin-selected function o f biolum inescence is conceivable for this species. The use o f light as burglar alarm signal has also been high lighted in dinoflagcllatcs (M cnsingcr Sc Case, 1992; Abraham s & Townsend, 1993), and suggested by Robison (1992) in the holothurian species E nypniastes eximia (Théel, 1882). In conclusion, this study illustrates the diversity of mechanism s involved in the use o f light as a defense against predation in brittle stars. This diversity should explain why this feature is so w idespread in the class Ophiuroidea. M oreover, besides the defensive function, it w ould b e v ery in terestin g to study oth er roles o f biolum inescence (such as help for predation or intraspecific com m unication...) in this class to increase the information concerning the function o f biolum inescence in brittle stars. A cknow ledgem ents This project was financially supported by the ASSEM BLE program m e o f the European Community, grant agreement no. 227799, for the access to the M arine Station Arago o f Banyul.s-sur-M.er. The authors also thank the University o f Santa B arbara for collaboration in the sam pling o f 0 . californica. This w ork was supported by a grant from de F N R S -F R IA to A. Jones. J. M allefet is a research associate o f the FN RS. This is a contribution to the Biodiversity R esearch Center (BDIV). References A b ra h a m s M.V. & T ow n sen d L.D . 1993. B iolum inescence in dinoñag eilates - a test o f the burglar alarm hypothesis. Ecology, 74: 258-260. De C o ck R . & M a tth y se n E, 2001. Do glow -w orm larvae (C o leo p tera : L am pyridae) use w arn in g coloration? Evolutionary* Ecology, 13: 619-639. D e C o c k R . & M a tth y s e n E . 2003. G lo w -w o rm larvae biolum inescence (C oleoptera : Lam pyridae) operates as an aposem atic signal upon toads (Bufo bufo). B ehavioral Ecology, 14: 103-108. D uffy E ., P e n n D., B o tton M ., B ro c k m a n n H . & L o v elan d R . 20Ö6. E ye and claspcr damage influence m ale m ating tactics in the horseshoe crab, Limulus'polyphem us. J o u rn a l o f E thology 24: 67-74. E isn e r T. & G r a n t R. 1981. Toxicity, odor aversion, an d olfacto ry aposem atism . Science, 213: 476-476. F o n ta in e A .R . 1964. The integum entary m ucous secretions o f the o p h iu ro id O phiocom ina nigra. J o u rn a l o f th e M a r in e Biological Association o f the United Kingdom , 44: 145- 162 . G ro b e r M . 1988. B rittle-star biolum inescence functions as an aposem atic signal to deter crustacean p red ato rs. A n im a l B ehaviour, 36: 493-501. G ro b e r M . 1989. B iolum inescent aposem atism - A reply to G uilford Sc Cuthill. Anim al Behaviour, 37: 341-343. G u ilfo rd T. & C u th ill L 1989. A p o se m a tism an d biolum inescence. A nim al behaviour, 37: 339-341. G u ilfo rd T. & D aw kins M. 1993. Are warning colors handicaps? Evolution, 47: 400-416. H a d d o c k S., M o lin e M . & C ase J . 2010. B iolum inescence in the sea. A nnual review o f M arine Science, 2: 443-493. H e rrin g P .J. 1995. B iolum incsccnt cch in o d erm s: u n ity o f function in diversity o f expression? In: E ch in o d en n Research Î9 9 5 (R. Emson, A.B. Smith Sc A.C. Cam pbell eds). A.A. Balkem a: Rotterdam. Jo n es A. & M allefet J . 2010. Abstracts o f the 16th International Sym posium on B iolum inescence and C h em ilum inescence • (ISBC 2010). Luminescence, 25; 155-156, L e im a r O ., E n q u ist M ., S iilen tu llb erg B. 1986. E volutionary stability o f aposematic coloration and prey im profitability - A theoretical analysis. Am erican N aturalist, 128: 469-490. M allefet 2012. Luminous brittle stars: an updated list. A bstract o f ¡ 4 ^ International E chinodenn Conference, B russels, 122 pp. M a re k P., P a p a j D., Y eager J ., M olina S, & M o o re W . 2011. B iolum inescent aposem atism in millipedes. Current B iology. 21:6 8 0 -6 8 1 . M en sin g er A. & C ase J. 1992. D inoflagellate lum inescence increases susceptibility o f Zooplankton to teleost predation. M arine B iology, 112: 2Ö7-210. M u n tz L ., E b lin g F. & K itc h in g J. 1965. T h e ecology o f lough ine. Journal o f Anim al E cology, 34; 315-329. R o b iso n B. .1992. B iolum inescence in th e b e n th o p clag ic H olothurian E nypiastes e+xim ia. Jo u rn a l o f th e M arine B iological Association o f the United K ingdom , 72: 463-472. S peed M . & R u x to n G . 2005. A posem atism : w hat should our starting point be? Proceedings o f the R o y a l S o ciety B~ Biological Sciences, 272: 431-438, StÖhr S. & O ’H a ra T. 2012. World O phiuroidea D atabase. Available online at http://w w w .m arinespecies.org/ophiuroidea. Consulted o n A ugust 2012.