Marine Biology

, Volume 150, Issue 5, pp 797–806 | Cite as

Newly metamorphosed Elysia clarki juveniles feed on and sequester chloroplasts from algal species different from those utilized by adult slugs

  • Nicholas E. Curtis
  • Sidney K. PierceEmail author
  • Steven E. Massey
  • Julie A. Schwartz
  • Timothy K. Maugel
Research Article


The adult, sacoglossan sea slug, Elysia clarki (Pierce et al. in Molluscan Res 26, 2006), sequesters functional chloroplasts in cells of the digestive diverticula from four species of macroalgae in the order Bryopsidales (Penicillus capitatus, Penicillus lamourouxii, Halimeda incrassata, and Halimeda monile). Feeding experiments were conducted in December, 2003, using individuals raised in the laboratory from egg masses laid by E. clarki adults which had been collected from Grassy Key, Florida, USA, and 29 species of macroalgae collected from the Florida Keys, Tampa Bay, Tarpon Springs, Florida, or Woods Hole, Massachusetts or obtained from the Culture Collection of Algae at the University of Texas at Austin, Texas. For the first 14-day post-metamorphosis, juveniles ate only the thin filamentous species, Bryopsis plumosa or Derbesia tenuissima. Transmission electron microscopy showed that the chloroplasts from both algae were sequestered intracellularly in juvenile slugs. Individuals offered any other macroalga, including the four species fed on by adults, did not feed on or incorporate any chloroplasts, and soon died. Juveniles switched from B. plumosa to P. capitatus at a length of ∼ 1.0 cm, and fixed for microscopy 14 days later had intact intracellular chloroplasts from both algae. Nucleotide sequences of the chloroplast gene, rbcL, from DNA extracted from E. clarki, collected from Vaca Key, Florida, were aligned with 22 other available macroalgal rbcL sequences indicating that these E. clarki adults had fed on three species of algae in the Bryopsidales including Bryopsis pennata, and TEM results partially confirmed this conclusion.


rbcL Algal Species Halimeda Digestive Cell rbcL Sequence 
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.



Specimens were collected under permits issued to SKP by the State of Florida. This work was supported by NSF grant #IBN 0315227. We thank Betty Loraamm for help with electron microscopy and Kathleen Hotchkiss for assistance with the figures. All experiments were conducted in compliance with the current laws of the United States of America.


  1. Brandley B (1984) Aspects of the ecology and physiology of Elysia cf. furvacauda (Mollusca: Sacoglossa). Bull Mar Sci 34:207–219Google Scholar
  2. Curtis NE, Massey SE, Schwartz JA, Tagihof H, Pierce SK (2004) The intracellular, functional chloroplasts in adult Elysia crispata come from several algal species, and are different from those in juvenile slugs. Integr Comp Biol 44:686Google Scholar
  3. Curtis NE, Massey SE, Pierce SK (2006) The symbiotic chloroplasts in the sacoglossan Elysia clarki are from several algal species. Invertebr Biol (in press)Google Scholar
  4. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  5. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  6. Jensen KR (1981) Observations on feeding methods in some Florida ascoglossans. J Moll Stud 47:190–199Google Scholar
  7. Jensen KR (1983) Factors affecting feeding selectivity in herbivorous ascoglossa (Mollusca: Opistobranchia). J Exp Mar Biol Ecol 66:135–148CrossRefGoogle Scholar
  8. Jensen KR (1993) Morphological adaptations and plasticity of radular teeth of the Sacoglossa ( = Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biol J Linn Soc 48:135–155CrossRefGoogle Scholar
  9. Mondy WL, Pierce SK (2003) Apoptotic-like morphology is associated with annual synchronized death in kleptoplastic sea slugs (Elysia crispata). Invertebr Biol 122:126–137CrossRefGoogle Scholar
  10. Pierce SK, Biron RW, Rumpho ME (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol 199:2323–2330PubMedGoogle Scholar
  11. Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204:237–240CrossRefGoogle Scholar
  12. Pierce SK, Curtis NE, Massey SE, Bass AL, Karl SA, Finney CM (2006) A morphological and molecular comparison between Elysia crispata and a new species of kleptoplastic sacoglossan sea slug (Gastropoda: Opisthobranchia) from the Florida Keys, USA Molluscan Res 26:23–38Google Scholar
  13. Pombert JF, Otis C, Lemieux C, Turmel M (2005) The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol 22:1903–1918CrossRefGoogle Scholar
  14. Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  15. Thorne JL, Kishino H, Felsenstein J (1992) Inching toward reality: an improved likelihood model of sequence evolution. J Mol Evol 34:3–16CrossRefGoogle Scholar
  16. Trench RK, Boyle JE, Smith DC (1973) The association between chloroplasts of Codium fragile and the mollusc Elysia viridis II. Chloroplast ultrastructure and photosynthetic carbon fixation in E. viridis Proc R Soc Lond B 184:63–81CrossRefGoogle Scholar
  17. Trowbridge CD (2000) The missing links: larval and post-larval development of the ascoglossan opistobranch Elysia viridis. J Mar Biol Assoc UK 80:1087–1094CrossRefGoogle Scholar
  18. Trowbridge CD, Todd CD (2001) Host–plant change in marine specialist herbivores: ascoglossan sea slugs on introduced macroalgae. Ecol Monogr 71:219–243CrossRefGoogle Scholar
  19. West HH, Harrigan JF, Pierce SK (1984) Hybridization of two populations of a marine opistobranch with different developmental patterns. Veliger 26:199–206Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Nicholas E. Curtis
    • 1
  • Sidney K. Pierce
    • 1
    Email author
  • Steven E. Massey
    • 1
  • Julie A. Schwartz
    • 1
  • Timothy K. Maugel
    • 2
  1. 1.Department of BiologyUniversity of South FloridaTampaUSA
  2. 2.Department of BiologyUniversity of MarylandCollege ParkUSA

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