Marine Biology

, Volume 151, Issue 1, pp 85–97 | Cite as

Uncommon diversity in developmental mode and larval form in the genus Macrophiothrix (Echinodermata: Ophiuroidea)

  • Jonathan D. Allen
  • Robert D. PodolskyEmail author
Research Article


Development mode in the ophiuroid genus Macrophiothrix includes an unusual diversity of planktonic larval forms and feeding types. The modes of development for seven congeners that coexist in coral reef habitats at Lizard Island, Australia were compared using larvae generated from crosses over several reproductive seasons from 1999 to 2003. Three species (Macrophiothrix koehleri Clark, Macrophiothrix longipeda Lamarck, Macrophiothrix lorioli Clark) develop from small eggs (<170 μm) into typical obligately feeding planktonic (planktotrophic) pluteus larvae with four larval arm pairs. The remaining four species develop from larger eggs (≥230 μm) into either facultatively-feeding or non-feeding (lecithotrophic) larval forms. The facultative planktotroph (Macrophiothrix rhabdota Clark) retains the ability to digest and benefit from food but does not require particulate food to complete metamorphosis. Among the lecithotrophic species, Macrophiothrix caenosa Hoggett retains the pluteus morphology with four pairs of larval arms, but is incapable of feeding, depending instead on maternal provisions for larval development. The remaining two lecithotrophs have simplified larval morphologies with only a single pair of full length (Macrophiothrix nereidina Lamarck) or highly reduced (Macrophiothrix belli Doderlein) larval arms and no functional mouth or gut. This genus includes the first example of facultative planktotrophy in ophiuroids, the first example in echinoderms of a complete pluteus morphology retained by a lecithotrophic larva, and three degrees of morphological simplification among lecithotrophic larval forms. Egg volume varies 20-fold among species and is related to variation in feeding mode, larval form, and development time, as predicted for the transition from planktotrophic to lecithotrophic development.


Larval Form Larval Body Ciliated Band Larval Culture Unfed Larva 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank J. Mader and J. McAlister for extensive assistance and discussions, R. Miller, K. Kemp, G. Howarth, R. Lynch, D. Allen, L. Hawkins, L. Haycock, B. Hazel, M. Pizer and T. Holtz for aid with adult brittlestar collection and larval culture, and D. Gupta for help with larval measurements. We thank the directors of the Lizard Island Research Station, A. Hoggett and L. Vail, for generous research space and logistical support. The manuscript was improved by comments from J. Grassle and two anonymous reviewers. Funding was provided by the PADI foundation and by National Science Foundation grant OCE-9811121. Collection, maintenance, and handling of brittlestars conformed with permits issued by the Great Barrier Reef Marine Park Authority.


  1. Alatalo P, Berg CJJ, D’Asaro CN (1984) Reproduction and development in the lucinid clam Codakia orbicularis. Bull Mar Sci 34:424–434Google Scholar
  2. Allen JA (1961) The development of Pandora inaequivalvis (Linne). J Embryol Exp Morphol 9:252–268PubMedGoogle Scholar
  3. Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequences. Mol Phylogenet Evol 6:425–437CrossRefGoogle Scholar
  4. Berg CJ Jr, Alatalo P (1982) Reproductive strategies of bivalve mollusks from deep-sea hydrothermal vents and intertidal sulfide-rich environments. Biol Bull 163:397Google Scholar
  5. Chia FS (1974) Classification and adaptive significance of developmental patterns in marine invertebrates. Thalass Jugosl 10:121–130Google Scholar
  6. Crofts DR (1937) The development of Haliotis tuberculata with special reference to organogenesis during torsion. Phil Trans R Soc Lond B 228:219–268CrossRefGoogle Scholar
  7. Crump ML (1989) Life history consequences of feeding versus non-feeding in a facultatively non-feeding toad larva. Oecologia 78:486–489CrossRefGoogle Scholar
  8. Doughty P (2002) Coevolution of developmental plasticity and large egg size in Crinia georgiana tadpoles. Copeia 4:928–937CrossRefGoogle Scholar
  9. Emlet RB (1986) Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus and a comparison with obligate planktotrophy in Clypeaster subdepressus (Clypeasteroida Echinoidea). J Exp Mar Biol Ecol 95:183–202CrossRefGoogle Scholar
  10. Emlet RB (1994) Body form and patterns of ciliation in nonfeeding larvae of echinoderms: functional solutions to swimming in the plankton? Am Zool 34:570–585CrossRefGoogle Scholar
  11. Emlet RB (1995) Developmental mode and species geographic range in regular sea urchins (Echinodermata: Echinoidea). Evolution 49:476–498CrossRefGoogle Scholar
  12. Emlet RB, McEdward LR, Strathmann RR (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol 2. A. A. Balkema, Rotterdam, pp 55–136Google Scholar
  13. Fell HB (1945) A revision of the current theory of echinoderm embryology. Trans Proc N Z Inst 75:73–101Google Scholar
  14. Fenaux L (1963) Note preliminaire sur le developpement larvaire de Amphiura chiajei (Forbes). Vie Milieu 14:91–96Google Scholar
  15. Grave C (1916) Ophiura brevispina. II. An embryological contribution and a study of the effect of yolk substance upon development and developmental processes. J Morphol 27:413–451CrossRefGoogle Scholar
  16. Grunbaum D, Strathmann RR (2003) Form, performance and trade-offs in swimming and stability of armed larvae. J Mar Res 61:659–691CrossRefGoogle Scholar
  17. Hart MW (1996a) Variation in suspension feeding rates among larvae of some temperate, eastern pacific echinoderms. Invertebr Biol 115:30–45CrossRefGoogle Scholar
  18. Hart MW (1996b) Evolutionary loss of larval feeding: development, form, and function in a facultatively feeding larva, Brisaster latifrons. Evolution 50:174–187CrossRefGoogle Scholar
  19. Hart MW (2000) Phylogenetic analyses of mode of larval development. Sem Cell Dev Biol 11:411–418CrossRefGoogle Scholar
  20. Hart MW, Podolsky RD (2005) Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars. Mol Phylogenet Evol 34:438–447CrossRefGoogle Scholar
  21. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51:1848–1861CrossRefGoogle Scholar
  22. Hendler G (1975) Adaptational significance of the patterns of ophiuroid development. Am Zool 15:691–715CrossRefGoogle Scholar
  23. Hendler G (1977) Development of Amphioplus abditus Echinodermata Ophiuroidea. Part 1: larval biology. Biol Bull 152:51–63CrossRefGoogle Scholar
  24. Hendler G (1979) Reproductive periodicity of ophiuroids (Echinodermata: Ophiuroidea) on the Atlantic and Pacific coasts of Panama. In: Stancyk SE (ed) Reproductive ecology of marine invertebrates. University of South Carolina Press, Columbia, pp 145–156Google Scholar
  25. Hendler G (1982) An echinoderm vitellaria with a bilateral larval skeleton: evidence for the evolution of ophiuroid vitellariae from ophioplutei. Biol Bull 163:405–530CrossRefGoogle Scholar
  26. Hendler G (1991) Echinodermata: Ophiuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Echinoderms and lophophorates, vol VI. Boxwood Press, Pacific Grove, pp 356–511Google Scholar
  27. Hoggett A (1990) Taxonomy and systematic position of the brittlestar genus Macrophiothrix H. L. Clark (Echinodermata: Ophiuroidea). Dissertation, Brisbane, AustraliaGoogle Scholar
  28. Hoggett AK (1991) The genus Macrophiothrix (Ophiuroidae: Ophiotrichidae) in Australian waters. Invertebr Taxon 4:1077–1146CrossRefGoogle Scholar
  29. Jeffery CH, Emlet RB (2003) Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the tertiary of southern Australia. Evolution 57:1031–1048CrossRefGoogle Scholar
  30. Jeffery WR, Swalla BJ (1992) Evolution of alternate modes of development in ascidians. Bioessays 14:219–226CrossRefGoogle Scholar
  31. Kelman D, Emlet RB (1999) Swimming and buoyancy in ontogenetic stages of the cushion star Pteraster tesselatus (Echinodermata: Asteroidea) and their implications for distribution and movement. Biol Bull 197:309–314CrossRefGoogle Scholar
  32. Kempf SC, Hadfield MG (1985) Planktotrophy by the lecithotrophic larvae of a nudibranch Phestilla sibogae Gastropoda. Biol Bull 169:119–130CrossRefGoogle Scholar
  33. Kempf SC, Todd CD (1989) Feeding potential in the lecithotrophic larvae of Adalaria proxima and Tritonia hombergi: an evolutionary perspective. J Mar Biol Assoc UK 69:659–682CrossRefGoogle Scholar
  34. Knowlton RE (1973) Larval development of the snapping shrimp Alpheus heterochaelis Say, reared in the laboratory. J Nat Hist 7:273–306CrossRefGoogle Scholar
  35. Kohn JA, Perron FE (1994) Life history and biogeography: patterns in Conus. Oxford University Press, OxfordGoogle Scholar
  36. Komatsu M, Shosaku T (1993) Development of the brittle star, Ophioplocus japonicus H. L. Clark. I. Zool Sci (Tokyo) 10:295–306Google Scholar
  37. Levin LA, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 1–48Google Scholar
  38. Levitan DR (2000) Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids. Am Nat 156:175–192CrossRefGoogle Scholar
  39. MacBride EW (1907) The development of Ophiothrix fragilis. Q J Microsc Sci 51:557–606Google Scholar
  40. McEdward LR (1985) An apparatus for measuring and recording the depth dimension of microscopic organisms. Trans Am Microsc Soc 104:194–200CrossRefGoogle Scholar
  41. McEdward LR (1986a) Comparative morphometrics of echinoderm larvae. II. Larval size, shape, growth, and the scaling of feeding and metabolism in echinoplutei. J Exp Mar Biol Ecol 96:267–286CrossRefGoogle Scholar
  42. McEdward LR (1986b) Comparative morphometrics of echinoderm larvae. I. Some relationships between egg size and initial larval form in echinoids. J Exp Mar Biol Ecol 96:251–265CrossRefGoogle Scholar
  43. McEdward LR (1996) Experimental manipulation of parental investment in echinoid echinoderms. Am Zool 36:169–179CrossRefGoogle Scholar
  44. McEdward LR, Herrera JC (1999) Body form and skeletal morphometrics during larval development of the sea urchin Lytechinus variegatus Lamarck. J Exp Mar Biol Ecol 232:151–176CrossRefGoogle Scholar
  45. McEdward LR, Miner BG (2001) Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–1170CrossRefGoogle Scholar
  46. McMillan WO, Raff RA, Palumbi SR (1992) Population genetic consequences of developmental evolution in sea urchins (genus Heliocidaris). Evolution 46:1299–1312PubMedGoogle Scholar
  47. Miller SE (1993) Larval period and its influence on post-larval life history: comparison of lecithotrophy and facultative planktotrophy in the aeolid nudibranch Phestilla sibogae. Mar Biol 117:635–645CrossRefGoogle Scholar
  48. Mladenov PV (1979) Unusual lecithotrophic development of the Caribbean brittle-star Ophiotrix oerstedi. Mar Biol 55:55–62CrossRefGoogle Scholar
  49. Mladenov PV (1985) Development and metamorphosis of the brittle-star Ophiocoma pumila: evolutionary and ecological implications. Biol Bull 168:285–295CrossRefGoogle Scholar
  50. Morgan R, Jangoux M (2005) Larval morphometrics and influence of adults on settlement in the gregarious ophiuroid Ophiothrix fragilis (Echinodermata). Biol Bull 208:92–99CrossRefGoogle Scholar
  51. Mortensen T (1921) Studies of the development and larval forms of echinoderms. G. E. C. Gad, CopenhagenCrossRefGoogle Scholar
  52. Mortensen T (1938) Contributions to the study of the developmental and larval forms of echinoderms IV. Kong Danske Vidensk Selsk Skrift Nat Math Afd 9 Raekke 7:1–59Google Scholar
  53. Olson RR, Cameron JL, Young CM (1993) Larval development (with observations on spawning) of the pencil urchin Phyllacanthus imperialis: a new intermediate larval form? Biol Bull 185:77–85CrossRefGoogle Scholar
  54. Pernet B (2003) Persistent ancestral feeding structures in nonfeeding annelid larvae. Biol Bull 205:295–307CrossRefGoogle Scholar
  55. Perron FE (1981) Larval growth and metamorphosis of Conus (Gastropoda: Toxoglossa) in Hawaii. Pac Sci 35:25–38Google Scholar
  56. Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198CrossRefGoogle Scholar
  57. Scheltema RS (1986) On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bull Mar Sci 39:290–322Google Scholar
  58. Selvakumaraswamy P, Byrne M (2000a) Reproduction, spawning, and development of 5 ophiuroids from Australia and New Zealand. Invertebr Biol 119:394–402CrossRefGoogle Scholar
  59. Selvakumaraswamy P, Byrne M (2000b) Vestigial ophiopluteal structures in the lecithotrophic larvae of Ophionereis schayeri (Ophiuroidea). Biol Bull 198:379–386CrossRefGoogle Scholar
  60. Selvakumaraswamy P, Byrne M (2004) Metamorphosis and developmental evolution in Ophionereis (Echinodermata: Ophiuroidea). Mar Biol 145:87–99CrossRefGoogle Scholar
  61. Sewell MA, Young CM (1997) Are echinoderm egg size distributions biomodal? Biol Bull 193:297–305CrossRefGoogle Scholar
  62. Sinervo B, McEdward LR (1988) Developmental consequences of an evolutionary change in egg size: an experimental test. Evolution 42:885–899CrossRefGoogle Scholar
  63. Smiley S, McEuen FS, Chaffee C, Krishnan S (1991) Echinodermata: Holothuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Echinoderms and lophophorates, vol VI . Boxwood Press, Pacific Grove, pp 663–750Google Scholar
  64. Stancyk SE (1973) Development of Ophiolepis elegans (Echinodermata: Ophiuroidea) and its implications in the estuarine environment. Mar Biol 21:7–12CrossRefGoogle Scholar
  65. Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, SeattleGoogle Scholar
  66. Strathmann R (1974) The spread of sibling larvae of sedentary marine invertebrates. Am Nat 108:29–44CrossRefGoogle Scholar
  67. Strathmann RR (1985) Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annu Rev Ecol Syst 16:339–361CrossRefGoogle Scholar
  68. Strathmann RR (1988) Larvae, phylogeny and von Baer’s law. In: Paul CRC, Smith AB (eds) Echinoderm phylogeny and evolutionary biology. Oxford Scientific Publications and Liverpool Geological Society, Oxford, pp 53–68Google Scholar
  69. Strathmann RR, Eernisse DJ (1994) What molecular phylogenies tell us about the evolution of larval forms. Am Zool 34:502–512CrossRefGoogle Scholar
  70. Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45CrossRefGoogle Scholar
  71. Wray GA (1996) Parallel evolution of nonfeeding larvae in echinoids. Syst Biol 45:308–322CrossRefGoogle Scholar
  72. Yamashita M (1988) Involvement of cyclic AMP in initiating maturation of the brittle-star Amphipholis kochii oocytes: induction of oocyte maturation by inhibitors of cyclic nucleotide phosphodiesterase and activators of adenylate cyclase. Dev Biol 125:109–114CrossRefGoogle Scholar
  73. Young CM (1990) Larval ecology of marine invertebrates: a sesquicentennial history. Ophelia 32:1–48CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Biology, CB#3280University of North CarolinaChapel HillUSA
  2. 2.College of CharlestonGrice Marine LaboratoryCharlestonUSA

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