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Home , Echinus (sea urchin), Echinus esculentus, Psammechinus

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This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute.

Notice: ©1995 A. A. Balkema. This manuscript is an author version with the final publication available and may be cited as: Tyler, P., Young, C. M., & Serafy, K. (1995). Distribution, diet and reproduction in the genus : evidence for recent diversification? In R. Emson, A. Smith, & A. Campbell (Eds.), research 1995 (pp. 29-35). Rotterdam, : A.A. Balkema.

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Echinoderm Research 1995

R.H. EMSON, A.B. SMITH AND A.C. CAMPBELL

EDITORS PROCEEDINGS OF THE FOURTH EUROPEAN COLLOQUIUM LONDON// 10-13 APRIL 1995 Echinoderm Research 1995

Edited by ROLAND EMSON King's College London ANDREW SMITH The Natural History Museum, London ANDREW CAMPBELL Queen Mary and Westfield College, London

A.A.BALKEMA/ROTIERDAM/BROOKFIELD/1995 Echinoderm Research 1995, Emson, Smith & Campbell (eds) © 1995 Balkema. Rotterdam. ISBN 90 54 10 596 8 Distribution, diet and reproduction in the genus Echinus: Evidence for recent diversification?

Paul Tyler Department of Oceanography, University of Southampton, UK Craig M.Young Harbor Branch Oceanographic Institution, Ft. Pierce, Fla., USA Keith Serafy Department of Biology, Southampton College, Long Island University. NY., USA

ABSTRACT: The genus EchimJs is both speciose and widely distributed. Although first observed in the Pliocene deposits of Europe and North Africa it now has a centre of distribution in the North Atlantic with widely separated populations of individual occurring in the South Atlantic and Pacific Ocean. Although the dietary characteristics of species of Echinus are driven by local availability, the reproductive features show considerable conservatism with all species examined producing a small egg and a number of species showing seasonal reproduction. In this paper we present a conceptual model of how larvae of the genus Echinus may be dispersed and how this has lead to allopatric speciation. In sympatric populations we present a model of speciation based on the timing of spawning in relation to the spring phytoplankton bloom.

I INTRODUCTION acutus are found in Norwegian waters (Hagstrom & Lonning, 1961) and there may be considerable intra­ Sea urchins are prominent among icons used to specific variation in E. escu/entus (Hagstrom & represent the sea. In European waters this image is Lonning, 1964). E. esculentus formed the basis of a invariably , be it observed by the series of papers (Stott, 1931; Moore, 1934, 1935, first year undergraduate or the visitor to the curio 193 7) in which reproduction and behaviour were the shop in a seaside resort, although neither might central themes. In the post war years interest in E. recognise it by its latin name. Because Echinus esculentus as a scientific model declined as it was esculentus is found in the upper subtidal and even replaced as an experimental tool by echinoids found intertidally on low springs tides it has become the on the margins of the USA. best known species within the genus. The genus As deep sea exploration entered the quantitative Echinus, however, is one of the most speciose of sea phase in the 1960s interest was renewed in species of urchin genera comprising some 17 species Echinus as they were found to be one of the (Mortensen, 1943). Although the genus is believed dominant megafaunal groups at bathyal depths often to have originated in the Tethyan Sea (fossils are occurring in considerable numbers (Grassle et al, found in Pliocene deposits of England, Algeria and 1975; Gage et al, 1985; Hecker, 1990). This interest Italy (Mortensen, 1943)) it has a centre of was stimulated by their spatial distribution and how distribution in the North Atlantic although species they modified the sediment and thus structured the are found in the South Atlantic and the Pacific. infaunal community. Scientific interest in the genus has almost been Although covering a wide geographical and invariably confined, until recently, to Echinus vertical range all the species of Echinus examined to escu/entus. This species was the first of the genus to date have a number of morphological and have its larval development described (MacBride, physiological features in common irrespective of 1898) and in the early part of this century was used species and environment. The species of the genus in hybridisation experiments incorporating E. acutus, are recognized by the form of the primary tubercle E. elegans and (as E. on the interambulacral or ambulacral plates and the miliaris)(Shearer et al, 1914, Fuchs, 1914). shape of the test (Mortensen, 1927). The genus Naturally occurring hybrids of E. escu/entus and E. Echinus is separated from the confamilial genus

29 Paracenlrolus by the number of pores in the to bathyal depths off the eastern US (Fig. I). This ambulacral plates and from the genus Psammechinus species represents one of the dominant components (originally assigned to the genus Echinus) by the of the megabenthos over its depth range, being plates on the buccal membrane and the form of the found in canyon and non-canyon areas (Rowe, globiferous pedicellariae (Mortensen, 1927). 1971), with densities of up to 0.78 per m2 (Hecker, In this mini review we explore some of the 1990) with an aggregated spatial distribution characteristics of the genus Echinus that have come (Grassle et al, 197S). to light in recent years. The opportuntities to explore Also found down the east side of North america deep-sea areas, as well as the ability to devise and are E. gracilis (130 to 2SO m) from New England to conduct in vitro experiments, has given us a new Trinidad (Fig. 1), E. tylodes (270 to 810 m) from insight into the origin, distribution and ecology of Cape Cod to southern Florida (Fig. 2) and E. wallsi this group. We address three main aspects of the ( 460 to 2600 m) at a small number of stations in genus Echinus: the distribution of species, and deep water in the NW Atlantic (Fig. I) (Mortensen, compare diet and reproduction between species. 1943, Serafy & Fell, 198S). An exciting recent discovery is a specimen of Echinus found at the Lucky Strike hydrothermal vents on the Mid­ 2. DISTRIBUTION AND SPATIAL Atlantic Ridge (M. Sibuet, pers. comm.) VARIABILITY In the south Atlantic E. at/anticus is found on the isolated outposts of Ascension and St. Helena The genus Echinus has a cosmopolitan distribution between 37S and S20 m depth (Fig. 3). Off South although the centre of distribution appears to be in Afiica (Fig. 3) E. gilchrisli is found between SO and the North Atlantic. In the shallow waters of the NE SOO m and the related E. slenoporus being 'deep sea' Atlantic E. esculenlus is found from 0 to I 00 m the label to the specimens being illegible (Mortensen, depth from north to the southwest coast of 1943). In the Pacific E. lucidus is found off Japan at (Fig. I). The 'Ingolf record of this species 180 to 17SO m depth and E. multidenlatus at 113S from 1264 m appears to be an exception. m depth off the Kermadec Islands (Fig. 3). On the Taxonomically closely related species are E. east side of the Pacific E. euryporus is found at 31 S lenuispinus found from 130 to 200m depth off the m off the Chilean coast whilst E. anchislus is found Shetland Isles, west oflreland and Porcupine Bank at depths from 1890 to 241 S m (Fig. 3). (Fig. 1). E. melo is found throughout the western Mediterranean, down the NW African coast and on the Azores between 30 and 1100 m depth (Fig. 1). 3. DIET The varieties of E. acutus are found over much of the NW European shelf, the western Mediterranean De Ridder & Lawrence (1982) gave the most recent and the coast areas of NW Africa (Fig. 2). extensive review of the diet in echinoids known to Mortensen (1943) dwells at considerable length on that date. As might be expected diet, in part, these varieties. Of significance is E. acutus var reflected distribution. The shallower water species norvegicus which has the widest distribution such as E. escu/enlus, E. aculus and E. me/a fed on particularly offNW Europe between 20 and 1280 m a variety of plant and material as well as the depth. gut contents containing considerable amounts of Another species overlapping from the shelf into inorganic material. As well as being an agent of bathyal depths is E. elegans which over its bioerosion (Krumbein & van der Pers, 1974) geographic range ofLofoten to the Moroccan shelf Echinus esculentus, the dominant shallow water (Fig. 2) covers a depth range of SO to 1710 m grazer on hard substrata round the coasts of the UK although an upper bathyal distribution of 704 to has been shown to regulate both the biomass and 1210, as found in the Rockall Trough appears to be species diversity in forests (Kain & Jones, more typical. (Gage et al, 198S). Further down the 1966). Unpublished data (Moore & Emson pers. slope is E. alexandri having a depth range of 1271 comm) have shown that in E. esculentus the type of to 2300 m (Fig. 2) but this species is confined to the food significantly affects the development of the NE Atlantic. A more cosmopolitan distribution at gonads. Moving into deeper water the varied diet these depths is seen in E. affinis ( 160S to 24SO m associated with Echinus becomes, apparently, more depth) which extends from the NE Atlantic, as far monotonous consisting of foram ooze and 'bottom south as the Bay of Biscay, on the Mid-Atlantic mud' (Mortensen, 1943; de Ridder & Lawrence, Ridge south of Iceland (Copley et al in submission) 1982). This simplicity of description belies the varied

30 120. so· 4o·w o· 40. E

Figure l . Distribution of Echinus esculentus, E. tenuispinus, E. melo, E. affinis, E. wallsi, E. gracilis and ?Echinus vent species in the North Atlantic and Mediterranean.

Table l. Known reproductive variables of the species of the genus Echinus.

Species Depth Reproductive comments Reference

Ecltinus esculentus 0 to 100(?1260)m Small eggs, seasonally produced, spawning varies with latitude Nichols et al 1985 Comley & Ansell, 1989 Ecllinus a/ji11is 1605 to 2450m Small eggs, seasonally breedin g, spawning in late winter Tyler & Gage, 1985 Eclli11us alexandri 1271 to 2300m Small eggs Monensen, 1943 Echinus acutus var norvegicus 20 to !280m Small eggs, seasonall y breeding Gage et al, 1986 EcllillliS elegans 704 to \210m Small eggs, seasonally breeding Gage et al, 1986 Ecllinus te/IIISipiiiUS 130 to 200m No information EclrillliS melo 30 to IIOOm No information EcllillliS wallsi 460 to 2600 No information Eclrillus gracilis \30 to 250m Small eggs Monensen, 194 3; Serafy & Fell, 1985 Echi1111S tylodes 270 to 8\0 Small eggs Monensen, 1943 Echii!IIS lucidus 180 to 1750m Small eggs Monensen, 1943 Eclli11us gilclrristi 50 to 500m Small eggs Monensen 194 3 Echimrs at/anticus 375 to 520m No information Eclritws multidel!tatlls !135m No information Ec llil!us euryporus 315m No information F.cltiiiiiS anclristus 1890 to 2415m No information Eclrinus ste11oporrrs 'deep sea' Small eggs Monensen, 1943

31 Figure 2. Distribution of Echinus elegans, E. a/exandri, E. tylodes and the varieties of E.acutus in the North Atlantic and Mediterranean.

~~_,_n\C Echinus multidentatus !135m . ~ 0

r:J J * * Echinus stenoporus 'deep sea' // Echinus gilchristi 50 to 500m * Echinus at/anticus 375 to 520m Echinus euryporus 3 15m ..&. Echinus anchistus 1890 to 2415m

Figure 3. Distribution of Echinus species in the South Atlantic and Pacific Oceans.

32 diet observed in the deep sea echinoid Echinus of E. acutus var norvegicus developed at pressures a/finis (Campos-Creasey et al, 1994). Although a up to lSOatm h.u1 the embryos of E. a/finis required deposit feeder careful analysis of the gut contents high pressure for successful early embryogenesis and showed this species contained a variety of failed to develop at lower pressures (Young & Tyler, phytoplanktonic organisms, including diatom spores 1993; Tyler et al in prep.). and coccolithophores, from surface primary The population structure of Echinus species has production. This 'phytodetrital' material has a strong been difficult to determine owing to the poor seasonal signal (Billett et al, 1983) and this is collection of newly recruited juveniles to shallow and reflected in the gut contents of E. a/finis. deep water adult populations. Juveniles of E. esculentus have been particularly difficult to find (D. Nichols pers. comm) and juveniles of the deep sea 4. REPRODUCTION species E. a/finis and E. elegans as well as upper bathyal E. acutus var norvegicus have only been One of the most distinctive features of the species collected in epibenthic sledge hauls (Gage & Tyler, within the genus Echinus is the gametogenic cycle. 1985; Gage et al 1986). These hauls suggest a Irrespective of both species and depth all individuals recruitment of Echinus juveniles to the adult examined to date (Table l) have a gametogenic population in the summer months but because of the cycle that shows a seasonal pattern of oocyte and lack of development of pedicellariae it is difficult to sperm development, with reduction division in the determine which species the juveniles represent in ovary occurring prior to spawning (Tyler & Gage, these hauls. The seasonal pattern seen in these 1984; Nichols et al 1985; Gage et al 1986; Comely species is supported by the growth marks observed & Ansell, 1990). The only variation in this in the interambulacral plates of E. esculentus and E. gametogenic cycle is the time of year of spawning a/finis interpreted as annual growth lines (Gage & with the deep-sea Echinus a/finis spawning in Tyler, 1985; Gage, 1992). February/March of each year (Tyler & Gage, 1984), the slightly shallower Echinus elegans and the shelf/upper bathyal species Echinus acutus var 5. DISCUSSION norvegicus a little later (Gage et al, 1986) and the shallow water Echinus esculentus in the late spring These data have led to the suggestion that speciation or early summer depending on geographic location in the genus Echinus may be a relatively recent (Nichols et al, 1985; Comely & Ansell, 1990). All phenomena (Tyler & Young, 1993). The fossil species produce a similar sized ovum ( -1 OOJi.m record of this genus is limited to the Pliocene and diameter) indicative ofplanktotrophic development later although it should be noted that shallow water (Table I). The larvae of Echinus esculentus and species of Echinus inhabit rocky substrata and are Echinus acutus have been described (McBride, thus less liable to fossilization (Smith, 1992). We 1898; Chadwick, 1914; Shearer et al, 1914) but the suggest the present distribution of the genus Echinus larva of the slope and deeper water species of represents possible variation in hydrographic events Echinus have yet to be identified. In addition there associated with the glaciallinterglacial cycles. For the has been considerable experimental hybridization shallow water species of Echinus the movement of between Echinus esculentus, Echinus acutus and the the polar front northwards allowed colonisation of closely related Psammechinus miliaris (then Echinus areas such as the Norwegian coast previously miliaris) (Shearer et al, 1914). covered by ice. The planktonic larvae produced by One of the main physiological variations E. esculentus could be transported northwards by between species of Echinus is the response of early the N. Atlantic Drift that bathes and warms the embryos to pressure. In a series of experiments coasts of northwest Europe. The shallow-water newly fertilized eggs of E. esculentus, E. acutus var species of Echinus have failed to colonise the coast norvegicus, E. affinis and Psammechinus miliaris of Greenland possibly because the hydrographic were subjected to pressures of l, 50, I 00, and pattern would take larvae into an area not 200atm (corresponding to surface, 500, I 000 and conducive to their survival. As the polar front moved 2000m depth). The results show that at pressures northwards the phytodetrital material from surface >SOatm the fertilized eggs of shallow living E. primary production formed a food source for the escu/entus and P. mi/iaris failed to develop, the eggs developing echinoplutei.

33 Although we do not yet understand the Although this distributional hypothesis may mechanism by which the genus Echinus invaded the explain speciation of Echinus on a cosmopolitan deep sea we believe its gametogenic and spawning basis it does not explain the speciation at the cycle are related to the arrival of phytodetrital apparent centre of distribution in the North Atlantic. material from surface primary production. The The clue may lie in the pressure adaptation of the allopatric populations of species of Echinus in the embryos. Embryos of E. acutus show the greatest deep sea suggest there may have been a dispersal depth tolerence and Mortensen ( 1943) implies this related to the past hydrography of the deep ocean. species is central to the evolution of Echinus. The formation of North Atlantic Deep Water Sympatric speciation may have occurred owing to (NADW) in the Norwegian Sea flows throughout reproductive isolation related to the timing of the worlds oceans to eventually reach the North spawning in shallow and deep water populations. E. Pacific. The formation of this water is known to vary affinis spawns considerably earlier than E. according to prevailing glacial or interglacial esculentus but the larvae of both species benefit conditions the results water movement being more from spring phytoplankton production. There is no rapid during interglacial periods (McCave et al , evidence that reproductive isolation in the species of 1995). As NADW sinks it flows along the Echinus was driven by changes in egg/sperm continental slope (as the Western Boundary recognition as natural and experimental hybridization Undercurrent) of the eastern margin of North between E. esculentus and E. acutus, and P. miliaris America. During the present interglacial this water has been known since early in the century (Shearer mass flows at a rate of 5 to 20 m sec·• . The most et al, 1914; Mortensen 1927 p.298). Variation in the recent evidence suggests mean flow is to the lower timing of reproduction is a stong selector for end of this range (Rhein, 1994). From previous data sympatric speciation and there is evidence the same of the time of spawning to the time of first patterm may be seen in the shallow and deep water recruitment of E. affinis (Gage & Tyler, 1985) we populations of the ophiuroid genus Ophiura and the estimate a minimum larval life of 89 days. This astropectinid seastars. appears to be a short larval life compared to the maximum known for Strongylocentrotus droebachiensis (152 days) and Allocentrotus fragilis REFERENCES (252 days)(Strathmann, 1978). A conservative estimate of the distance travelled in a unidirectional Billett, D.S.M., R.S. Lampitt, A.L. Rice & R.F.C. Oow (assumed) by larvae of E. affinis would be 370 Mantoura (1983) Seasonal sedimentation of km. An estimate of 1700 km may not be unrealistic phytoplankton to the deep sea benthos. Nature considering echinoid larvae have been found in 302, 520-522 equatorial currents in the middle of the Atlantic Campos-Creasey, L.S., P.A. Tyler, J.D. Gage & Ocean (Scheltema, 1977). With these data in mind A.W.G. John (1994) Vertical flux coupled to we suggest that the flow of NADW (particularly the diet and seasonal life history of the deep-sea during interglacial periods) was capable of echinoid Echinus affinis. Deep-Sea Res. 41 , transporting larvae that eventally settled at bathyal 369-388 depths off South Mrica, off the Kermedac Islands Chadwick, H.C. 1914 Echinoderm Larvae. LMBC and off Japan. Reduced flow during glacial periods Memoirs XXII. may have allowed allopatric speciation to have Comley, C.A. & A.D. Ansell (1990) The occurred at these sites. The occurrence of two reproductive cycle of Echinus esculentus L. on species of Echinus of Peru/Chile represents an the Scottish West Coast. Estuar. Coast. Shelf enigma. NADW does not enter this part of theSE Sci. 29, 385-407 Pacific. One pathway would have been through the de Ridder, C. & Lawrence, J.M. (1982) Food and Straits of Panama before the Isthmus of Panama feeding mechanisms: Echinoidea. In closed some 5m years ago. Certainly there has been '&hinoderm Nutrition' eds M. Jangoux & J.M. time for speciation since that time (see Bermingham Lawrence. Balkema, Rotterdam 57-115 & Lessios, 1993) although the Pliocene origin of the Fuchs, H.M. (1914) On F2 Echinus hybrids. J. Mar. genus Echinus mediates against this suggestion . A Bioi. Ass. U.K. 10, 464-465 second possibility is the deep return flow of water Gage J.D. (1992a) Growth bands in the through the Drake Passage may have transported Echinus esculentus: Results from tetracycline- larvae into the SE Pacific.

34 mark/recapture. J. Mar. Bioi. Ass. UK. 12, 257- Moore, H.B. (1935) A comparison of the biology of 260 Echitms escu/entus in different habitats: Part II. Gage, J.D. ( 1992b) Natural growth bands and J Mar. Bioi. Ass. UK20, 109-128 growth variability in the sea urchin Echinus Moore, H. B. (1937)A comparison of the biology of esculentus: results from tetracycline tagging. Echinus escu/entus in different habitats: Part III. Mar. Bioi. 114, 607-616 J. Mar. Bioi. Ass. UK21, 711-720 Gage J.D, D.S.M. Billett, M. Jensen & P.A. Tyler Mortensen, T. (1927) Handbook of the Echinoderms ( 1985) Echinoderms of the Rockall Trough II of the British Isles. Oxford University Press Echinoidea and Holothurioidea. Bull Br. Mus. 471pp Nat Hist Zoo/. 48, 173-213 Mortensen, T. (1943) Monograph of the Echinoidea Gage J.D. & P.A. Tyler (1985) Growth and III C. A. Reitzel, Copenhagen recruitment in the sea urchin Echinus affinis. Nichols, D., G.M . Bishop & A.A.T. Sime (1985) Mar. Bioi. 90. 41-51 reproductive and nutritional periodicities in Gage, J.D., P.A. Tyler & D. Nichols (1986) populations of the European sea urchin Echinus Reproduction and growth of Echinus acutus var esculentus (Echinodermata: Echinoidea) from norvegicus and E. elegans on the continental the English Channel. J Mar. Bioi. Ass. UK 65, slope off . J Exp. Mar. Bioi. Ecol. 203-220 101,61-83 Rhein, M. (1994) The Deep Western Boundary Grassle, J.F., H.L. Sanders, R.R. Hessler, G.T. Current: tracers and velocities. Deep-Sea Res. Rowe & T McLellan ( 1975) Pattern and 41, 263-281 zonation: a study of the bathyal megafauna Rowe, G. T. ( 1971) Observations on bottom currents using the research submersible Alvin. Deep-Sea. and epibenthic populations in Hatteras Res. 22,457-481 submarine canyon. Deep-Sea Res. 18, 569-581 Hagstrom, B.E. & S. Lonning (1961) Morphological Scheltema, R.S. (1977)Dispersal of marine and experimental studies on the genus Echinus. organisms: paleobiogeographic and Sarsia 4, 21-31 biostratigraphic implications. In: Concepts and Hagstrom, B.E. & S. Lonning ( 1964) Morphological methods of biostratigraphy. eds E.G. Kauffman variation in Echinus escu/entus from the & I.E. Hazel. Dowden, Hutchinson & Ross Inc. Norwegian Coast. Sarsia 17, 39-46 Stroudsburg, P A pp 73-160 Hecker, B. (1990) Variation in megafauna! Seraty, D.K. & F. J. Fell (1985) Marine Flora and assemblages on the continental margin south of Fauna of the Northeastern United States. New England. Deep-Sea Res. 37, 37-57 Echinodermata: Echinoidea. NOAA Technical Kain, J.M. & N .L. Jones (1966) Algal colonization Report NMFS 33, 1-27 after the removal of Echinus. In 'Proceedings of Shearer, C., W. De Morgan & H.M. Fuchs (1914) the 5th International Seaweed Symposium. eds. On the experimental hybridization of echinoids. E.G. Young & J.M. McLaughlan, Pergammon, Phil. Trans. Roy. Soc. B. 204, 255-362 139-140 Smith A.B. ( 1992) Echinoderm phylogeny: Krumbein, W.E. & J.N.C. van der Poes (1977) morphology and molecules approach accord. Diving investigations on biodeterioration by the TREE 17: 224-229 sea urchin in the rocky sublittoral of Helgoland. Tyler, P.A. & J.D. Gage (1984) Seasonal He/g. wiss. Meers. 16, 1-17 reproduction of Echinus affinis McBride (1898) The development of echinoids I. (Echinodermata: Echinoidea) in the Rockall The larvae of Echinus miliaris and Echinus Trough, NE Atlantic Ocean. Deep-Sea Res. 31, esculentus. Quart. J. Micro. Soc. 42, p335 387-402 McCave, I.N., B. Manighetti & N.A.S. Beveridge Tyler P.A. , C.M. Young & J.D. Gage in prep ( 1995) Circulation of the North Atlantic inferred Pressure effects on early embryogenesis on from grain size measurements. Nature 374, 149- species of the genus Echinus from different 151 depths in the NE Atlantic Ocean. Moore, H.B. (1934) A comparison of the biology of Young C.M. & P.A. Tyler (1993) Embryos ofthe Echinus esculentus in different habitats: Part I. deep-sea echinoid Echinus affinis require high J. Mar. Bioi. Ass. UK 19, 869-885 pressure for development. Limnol. Oceanog. 38: 178-181

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