Marine Biology

, Volume 151, Issue 1, pp 301–311 | Cite as

Availability of dissolved organic matter offsets metabolic costs of a protracted larval period for Bugula neritina (Bryozoa)

  • Collin H. Johnson
  • Dean E. WendtEmail author
Original Article


For nearly a century researchers have investigated the uptake and utilization of dissolved organic matter (DOM) by marine invertebrates, but its contribution to their growth, reproduction, and survival remains unclear. Here, the benefit of DOM uptake was assessed for the marine bryozoan Bugula neritina (Linnaeus 1758) through performance comparisons of individuals in the presence and absence of DOM. The experiments were performed using B. neritina collected from floating docks in Beaufort, NC, USA from July to September 2004. Seawater was subjected to ultraviolet irradiation to reduce naturally occurring DOM, and then enriched with either 1 μM of palmitic acid or a mixture containing 1 μM each of glucose, alanine, aspartic acid and glycine. Larvae in DOM-enriched and DOM-reduced treatments were sampled and induced to metamorphose following 1, 6, 12, and 24 h of continuous swimming at 25°C. Sampled larvae were assessed for initiation of metamorphosis, completion of metamorphosis, and ancestrular lophophore size to determine the extent to which energy acquired from DOM uptake could offset the metabolic costs of prolonged larval swimming. DOM treatment had no significant effect on initiation of metamorphosis, but did have a significant effect on completion of metamorphosis and lophophore size. Larvae swimming in DOM-enriched treatments for 24 h experienced a 20% increase in metamorphic completion rate, compared to larvae swimming for 24 h in the DOM-reduced treatment. In addition, larvae in the amino acid and sugar mixture for 24 h had a significantly larger lophophore surface area and volume (23 and 31%, respectively), compared to larvae in DOM-depleted seawater. To ensure that the increases in performance found in larvae with access to DOM were not due to a decrease in metabolic activity, the respiration rates for these larvae were compared to those of larvae in DOM-depleted seawater. There were no significant differences between these treatments, indicating that the increases in performance were due to the energy acquired from DOM. These results clearly show that for B. neritina, DOM uptake results in increased metamorphic success and in the size of the feeding apparatus following an extended larval swimming duration.


Total Organic Carbon Dissolve Organic Matter Mixture Treatment Larva Swimming Energetic Reserve 
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 George Trevelyan (The Abalone Farm, Cayucos, CA) for graciously providing abalone larvae and technical assistance. Craig Carlson (UCSB) conducted the TOC analysis and provided suggestions improving the study. We also thank Dan Rittschof (Duke University Marine Lab) for allowing portions of this study to be conducted in his lab, and Beatriz Orihuela de Diaz for her technical assistance and procurement of adult colonies. We are grateful to Robert Smidt (California Polytechnic State University) for lending his expertise on statistical analysis. Two anonymous reviewers provided thoughtful comments improving this manuscript. Funding was provided by the National Science Foundation (Grant # IBN-0130634, awarded to D.E. Wendt), the Office of Naval Research (N00014-02-093, awarded to D.E. Wendt) and Cal Poly Student Fees.


  1. Aitkenhead-Peterson JA, McDowell WH, Neff JC (2003) Sources, production, and regulation of allocthonous dissolved organic matter inputs to surface waters. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 25–70CrossRefGoogle Scholar
  2. Armstrong FAJ, Tibbitts S (1968) Photochemical combustion of organic matter in sea water, for nitrogen, phosphorous and carbon determination. J Mar Biolog Assoc UK 48:143–152CrossRefGoogle Scholar
  3. Armstrong FAJ, Williams PM, Strickland DH (1966) Photo-oxidation of organic matter in sea water by ultra-violet radiation, analytical and other applications. Nature 211:481–483CrossRefGoogle Scholar
  4. Azam F, Hodson RE (1977) Size distribution and activity of marine microheterotrophs. Limnol Oceanogr 22:492–501CrossRefGoogle Scholar
  5. Beattie J, Bricker C, Garvin D (1961) Photolytic determination of trace amounts of organic material in water. Anal Chem 33:1890–1892CrossRefGoogle Scholar
  6. Ben-David-Zaslow R, Benayahu Y (2000) Biochemical composition, metabolism, and amino acid transport in planula-larvae of the soft coral Heteroxenia fuscescens. J Exp Zool 287:401–412CrossRefGoogle Scholar
  7. Benner R (2002) Chemical composition and reactivity. In: Hansell DA, Carlson CA (eds) Biogechemistry of marine dissolved organic matter. Academic, San Diego, pp 59–90CrossRefGoogle Scholar
  8. Benner R (2003) Molecular indicators of the bioavailability of dissolved organic matter. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 121–137CrossRefGoogle Scholar
  9. Best MA, Thorpe JP (1986) Effects of food particle concentration on feeding current velocity in six species of marine Bryozoa. Mar Biol 93:255–262CrossRefGoogle Scholar
  10. Carlson CA (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of dissolved organic matter in the ocean. Academic, San Diego, pp 91–151CrossRefGoogle Scholar
  11. Crawford CC, Hobbie JE, Webb KL (1974) The utilization of dissolved free amino acids by estuarine microorganisms. Ecology 55:551–563CrossRefGoogle Scholar
  12. Ferguson JC (1967) An autoradiographic study of the utilization of free exogenous amino acids by starfishes. Biol Bull 133:317–329CrossRefGoogle Scholar
  13. Ferguson JC (1980a) The non-dependency of a starfish on epidermal uptake of dissolved organic matter. Comp Biochem Physiol 66A:461–465CrossRefGoogle Scholar
  14. Ferguson JC (1980b) Fluxes of dissolved amino acids between sea water and Echinaster. Comp Biochem Physiol 65A:291–295CrossRefGoogle Scholar
  15. Ferguson JC (1982) A comparative study of the net metabolic benefits derived from the uptake and release of free amino acids by marine invertebrates. Biol Bull 162:1–17CrossRefGoogle Scholar
  16. Gatti S, Brey T, Müller WEG, Heilmayer O, Holst G (2002) Oxygen microoptodes: a new tool for oxygen measurements in aquatic animal ecology. Mar Biol 140:1075–1085CrossRefGoogle Scholar
  17. Jaeckle WB (1994) Rates of energy consumption and acquisition by lecithtrophic larvae of Bugula neritina (Bryozoa: Cheilostomata). Mar Biol 119:517–523CrossRefGoogle Scholar
  18. Jaeckle WB (1995) Transport and metabolism of alanine and palmitic acid by field-collected larvae of Tedania ignis (Porifera, Demospongiae): estimated consequences of limited label translocation. Biol Bull 189:159–167CrossRefGoogle Scholar
  19. Jaeckle WB, Manahan DT (1989) Feeding by a “nonfeeding” larva: uptake of dissolved amino acids from seawater by lecithotrophic larvae of the gastropod Haliotis rufescens. Mar Biol 103:87–94CrossRefGoogle Scholar
  20. Jørgensen CB (1976) August Pütter, August Krogh, and modern ideas on the use of dissolved organic matter in aquatic environments. Biol Rev 51:291–328CrossRefGoogle Scholar
  21. Kirchman DL (2003) The contribution of monomers and other low molecular weight compounds to the flux of DOM in aquatic ecosystems. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems: interactivity of dissolved organic matter. Academic, San Diego, pp 217–241CrossRefGoogle Scholar
  22. Klimant I, Meyer V, Kühl M (1995) Fiber-optic microsensors, a new tool in aquatic biology. Limnol Oceanogr 40:1159–1165CrossRefGoogle Scholar
  23. Maldanado M, Young CM (1999) Effects of the duration of larval life on postlarval stages of the demosponge Sigmadocia caerulea. J Exp Mar Biol Ecol 232:9–21CrossRefGoogle Scholar
  24. Manahan DT (1983) The uptake and metabolism of dissolved amino acids by bivalve larvae. Biol Bull 164:236–250CrossRefGoogle Scholar
  25. Manahan DT (1990) Adaptations by invertebrate larvae for nutrient acquisition from seawater. Am Zool 30:147–160CrossRefGoogle Scholar
  26. Manahan DT, Wright SH, Stephens GC, Rice MA (1982) Transport of dissolved amino acids by the mussel, Mytilus edulis: demonstration of net uptake from natural seawater. Science 215:1253–1255CrossRefGoogle Scholar
  27. Marsh AG, Manahan DT (1999) A method for accurate measurements of the respiration rates of marine invertebrate embryos and larvae. Mar Ecol Prog Ser 184:1–10CrossRefGoogle Scholar
  28. Neter J, Wasserman W, Kutner MH (1985) Applied linear statistical models: regression, analysis of variance, and experimental designs, 2nd edn. Richard D. Irwin, Inc, IllinoisGoogle Scholar
  29. Pechenik JA, Cerulli TR (1991) Influence of delayed metamorphosis on survival, growth, and reproduction of the marine polychaete Capitella sp. I. J Exp Mar Biol Ecol 151:17–27CrossRefGoogle Scholar
  30. Shick JM (1975) Uptake and utilization of dissolved glycine by Aurelia aurita scyphistomae: temperature effects on the uptake process; nutritional role of dissolved amino acids. Biol Bull 148:117–140CrossRefGoogle Scholar
  31. Shilling FM, Manahan DT (1994) Energy metabolism and amino acid transport during early development of Antarctic and temperate echinoderms. Biol Bull 187:398–407CrossRefGoogle Scholar
  32. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman and Co., New YorkGoogle Scholar
  33. Stephens GC (1962) Uptake of organic material by aquatic invertebrates. I. Uptake of glucose by the solitary coral, Fungia scutaria. Biol Bull 123:648–659CrossRefGoogle Scholar
  34. Stephens GC (1988) Epidermal amino acid transport in marine invertebrates. Biochim Biophys Acta 947:113–138CrossRefGoogle Scholar
  35. Stephens GC, Schinske RA (1961) Uptake of amino acids by marine invertebrates. Limnol Oceanogr 6:175–181CrossRefGoogle Scholar
  36. Strathman MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, SeattleGoogle Scholar
  37. Weast RC, Astle MJ (1980) CRC handbook of chemistry and physics, 61st edn. CRC Press, Boca RatonGoogle Scholar
  38. Wendt DE (1996) Effect of larval swimming duration on success of metamorphosis and size of the ancestrular lophophore in Bugula neritina (Bryozoa). Biol Bull 191:224–233CrossRefGoogle Scholar
  39. Wendt DE (1998) Effect of larval swimming duration on growth and reproduction of Bugula neritina (Bryozoa) under field conditions. Biol Bull 195:126–135CrossRefGoogle Scholar
  40. Wendt DE (2000) Energetics of larval swimming and metamorphosis in four species of Bugula (Bryozoa). Biol Bull 198:346–356CrossRefGoogle Scholar
  41. Wendt DE, Woollacott RM (1995) Induction of larval settlement by KCl in three species of Bugula (Bryozoa). Invert Biol 114:345–351CrossRefGoogle Scholar
  42. Williams PJlB, Berman T, Holm-Hansen O (1976) Amino acid uptake and respiration by marine heterotrophs. Mar Biol 35:41–47CrossRefGoogle Scholar
  43. Woollacott RM, Pechenik JA, Imbalzano KM (1989) Effects of duration of larval swimming period on early colony development in Bugula stolonifera (Bryozoa: Cheilostomata). Mar Biol 102:57–63CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Biological Sciences Department and Center for Coastal Marine SciencesCalifornia Polytechnic State UniversitySan Luis ObispoUSA
  2. 2.MCZ labsHarvard UniversityCambridgeUSA

Personalised recommendations