Mandibular Gnathobases of Marine Planktonic Copepods—Structural and Mechanical Challenges for Diatom Frustules

  • Jan MichelsEmail author
  • Stanislav N. Gorb
Part of the Biologically-Inspired Systems book series (BISY, volume 6)


Copepods are dominant members of the marine zooplankton. Their diets often contain considerable proportions of diatomtaxa, many of which are known for superior mechanical properties of their mineralised frustules. Nevertheless, many copepod species are able to efficiently crush these frustules including rather stable ones. This ability very likely requires feeding tools with specific shapes, material compositions and material properties. When ingesting food, the copepods use the gnathobases of their mandibles to grab and, if necessary, crush and mince the food items. The morphology of these gnathobases is related to the diets of the copepods. Gnathobases of copepod species that mainly feed on phytoplankton feature compact and stable tooth-like structures, so-called teeth. In several copepod species these gnathobase teeth have been found to contain silica. Recent studies revealed the existence of complex composite structures that, in addition to silica, are composed of the soft and elastic protein resilin and form siliceous gnathobase teeth with a rubber-like bearing. These composite structures very probably increase the efficiency of the siliceous teeth while simultaneously reducing the risk of their mechanical damage. They are supposed to have coevolved with the diatom frustules in an evolutionary arms race, and their development might have contributed considerably to the dominance of copepods within today’s marine zooplankton.


Zooplankton Copepod Gnathobase Mandible Composite Silica Resilin Stress Wear Evolutionary arms race Functional morphology 



This project was financially supported by the virtual institute ‘PlanktonTech’ of the Helmholtz Association. Sigrid Schiel kindly provided copepod samples, and Ruth Alheit helped with the sorting of the samples. The provision of the photograph showing the live Calanoides acutus specimen by Ingo Arndt is gratefully acknowledged. This book chapter is adapted from the publication ‘Michels J, Gorb SN (2015) Mandibular gnathobases of marine planktonic copepods—feeding tools with complex micro- and nanoscale composite architectures. Beilstein J Nanotechnol 6:674–685’.


  1. Andersen SO, Weis-Fogh T (1964) Resilin. A rubberlike protein in arthropod cuticle. Adv Insect Physiol 2:1–65CrossRefGoogle Scholar
  2. Anraku M, Omori M (1963) Preliminary survey of the relationship between the feeding habit and the structure of the mouth-parts of marine copepods. Limnol Oceanogr 8:116–126CrossRefGoogle Scholar
  3. Arashkevich YeG (1969) The food and feeding of copepods in the northwestern Pacific. Oceanology 9:695–709Google Scholar
  4. Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192CrossRefGoogle Scholar
  5. Bechstein K, Michels J, Vogt J, Schwartze GC, Vogt C (2011) Position-resolved determination of trace elements in mandibular gnathobases of the Antarctic copepod Calanoides acutus using a multimethod approach. Anal Bioanal Chem 399:501–508CrossRefGoogle Scholar
  6. Beklemishev KV (1954) The discovery of silicious formations in the epidermis of lower crustacea (in Russian). Dolk Akad Nauk SSSR 97:543–545 (english translation by McLean CA, Trans. 29, Ministry of Agriculture, Fisheries and Food)Google Scholar
  7. Bhushan B (2000) Modern tribology handbook, 2. CRC Press, Boca RatonCrossRefGoogle Scholar
  8. Brunner E, Richthammer P, Ehrlich H, Paasch S, Simon P, Ueberlein S, van Pée K-H (2009) Chitin-based organic networks: an integral part of cell wall biosilica in the diatom Thalassiosira pseudonana. Angew Chem Int Ed Engl 48:9724–9727CrossRefGoogle Scholar
  9. Bundy MH, Vanderploeg HA (2002) Detection and capture of inert particles by calanoid copepods: the role of the feeding current. J Plankton Res 24:215–223CrossRefGoogle Scholar
  10. Cribb BW, Stewart A, Huang H, Truss R, Noller B, Rasch R, Zalucki MP (2008) Insect mandibles—comparative mechanical properties and links with metal incorporation. Naturwissenschaften 95:17–23CrossRefGoogle Scholar
  11. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511CrossRefGoogle Scholar
  12. Ehrlich H (2010) Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev 52:661–699CrossRefGoogle Scholar
  13. Fowler SW, Fisher NS (1983) Viability of marine phytoplankton in zooplankton fecal pellets. Deep-Sea Res 30:963–969CrossRefGoogle Scholar
  14. Friedrichs L, Hörnig M, Schulze L, Bertram A, Jansen S, Hamm C (2013) Size and biomechanic properties of diatom frustules influence food uptake by copepods. Mar Ecol Prog Ser 481:41–51CrossRefGoogle Scholar
  15. Gibson LJ, Ashby MF (1988) Cellular solids: structure and properties. Pergamon Press, New YorkGoogle Scholar
  16. Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421:841–843CrossRefGoogle Scholar
  17. Hardy A (1970) The open sea. The world of plankton. Collins, LondonGoogle Scholar
  18. Hillerton JE, Robertson B, Vincent JFV (1984) The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles. J Stored Prod Res 20:133–137CrossRefGoogle Scholar
  19. Humes AG (1994) How many copepods? Hydrobiologia 292/293:1–7CrossRefGoogle Scholar
  20. Huys R, Boxshall GA (1991) Copepod evolution. The Ray Society, LondonGoogle Scholar
  21. Itoh K (1970) A consideration on feeding habits of planktonic copepods in relation to the structure of their oral parts. Bull Plankton Soc Japan 17:1–10Google Scholar
  22. Jansen S (2008) Copepods grazing on Coscinodiscus wailesii: a question of size? Helgol Mar Res 62:251–255CrossRefGoogle Scholar
  23. Kiørboe T (2011) What makes pelagic copepods so successful? J Plankt Res 33:677–685CrossRefGoogle Scholar
  24. Koehl MAR (2004) Biomechanics of microscopic appendages: functional shifts caused by changes in speed. J Biomech 37:789–795CrossRefGoogle Scholar
  25. Koehl MAR, Strickler JR (1981) Copepod feeding currents: food capture at low Reynolds number. Limnol Oceanogr 26:1062–1073CrossRefGoogle Scholar
  26. Longhurst AR (1985) The structure and evolution of plankton communities. Prog Oceanogr 15:1–35CrossRefGoogle Scholar
  27. Malkiel E, Sheng J, Katz J, Strickler JR (2003) The three-dimensional flow field generated by a feeding calanoid copepod measured using digital holography. J Exp Biol 206:3657–3666CrossRefGoogle Scholar
  28. Michels J (2007) Confocal laser scanning microscopy: using cuticular autofluorescence for high resolution morphological imaging in small crustaceans. J Microsc 227:1–7Google Scholar
  29. Michels J (2013) Confocal laser scanning microscopy—detailed three-dimensional morphological imaging of marine organisms. In: Reynaud EG (ed) Imaging marine life: macrophotography and microscopy approaches for marine biology. Wiley-VCH, Weinheim, pp 69–91Google Scholar
  30. Michels J, Büntzow M (2010) Assessment of Congo red as a fluorescence marker for the exoskeleton of small crustaceans and the cuticle of polychaetes. J Microsc 238:95–101Google Scholar
  31. Michels J, Gorb SN (2012) Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy. J Microsc 245:1–16Google Scholar
  32. Michels J, Schnack-Schiel SB (2005) Feeding in dominant Antarctic copepods—does the morphology of the mandibular gnathobases relate to diet? Mar Biol 146:483–495Google Scholar
  33. Michels J, Vogt J, Gorb SN (2012) Tools for crushing diatoms—opal teeth in copepods feature a rubber-like bearing composed of resilin. Sci Rep 2:465Google Scholar
  34. Michels J, Vogt J, Simon P, Gorb SN (2015) New insights into the complex architecture of siliceous copepod teeth. Zoology 118:141–146Google Scholar
  35. Miller CB, Nelson DM, Guillard RRL, Woodward BL (1980) Effects of media with low silicic acid concentrations on tooth formation in Acartia tonsa Dana (Copepoda, Calanoida). Biol Bull 159:349–363CrossRefGoogle Scholar
  36. Miller CB, Nelson DM, Weiss C, Soeldner AH (1990) Morphogenesis of opal teeth in calanoid copepods. Mar Biol 106:91–101CrossRefGoogle Scholar
  37. Nishida S, Ohtsuka S (1996) Specialized feeding mechanism in the pelagic copepod genus Heterorhabdus (Calanoida: Heterorhabdidae), with special reference to the mandibular tooth and labral glands. Mar Biol 126:619–632CrossRefGoogle Scholar
  38. Ohtsuka S, Onbé T (1991) Relationship between mouthpart structures and in situ feeding habits of species of the family Pontellidae (Copepoda: Calanoida). Mar Biol 111:213–225CrossRefGoogle Scholar
  39. Paffenhöfer G-A, Strickler JR, Alcaraz M (1982) Suspension-feeding by herbivorous calanoid copepods: a cinematographic study. Mar Biol 67:193–199CrossRefGoogle Scholar
  40. Pilson, MEQ (2012) An introduction to the chemistry of the sea, 2nd edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  41. Price HJ, Paffenhöfer G-A, Strickler JR (1983) Modes of cell capture in calanoid copepods. Limnol Oceanogr 28:116–123CrossRefGoogle Scholar
  42. Quicke DLJ, Wyeth P, Fawke JD, Basibuyuk HH, Vincent JFV (1998) Manganese and zinc in the ovipositors and mandibles of hymenopterous insects. Zool J Linn Soc Lond 124:387–396CrossRefGoogle Scholar
  43. Schnack SB (1989) Functional morphology of feeding appendages in calanoid copepods. In: Felgenhauer BE, Watling L, Thistle AB (eds) Functional morphology of feeding and grooming in Crustacea. Balkema, Rotterdam, pp 137–151Google Scholar
  44. Schofield RMS, Nesson MH, Richardson KA (2002) Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften 89:579–583Google Scholar
  45. Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32CrossRefGoogle Scholar
  46. Smetacek V (2001) A watery arms race. Nature 411:745CrossRefGoogle Scholar
  47. Strickler JR (1982) Calanoid copepods, feeding currents, and the role of gravity. Science 218:158–160CrossRefGoogle Scholar
  48. Sullivan BK, Miller CB, Peterson WT, Soeldner AH (1975) A scanning electron microscope study of the mandibular morphology of boreal copepods. Mar Biol 30:175–182CrossRefGoogle Scholar
  49. Tréguer P, Nelson DM, Van Bennekom AJ, DeMaster DJ, Leynaert A, Quéguiner B (1995) The silica balance in the world ocean: a reestimate. Science 268:375–379CrossRefGoogle Scholar
  50. Turner JT (1978) Scanning electron microscope investigations of feeding habits and mouthpart structures of three species of copepods of the family Pontellidae. Bull Mar Sci 28:487–500Google Scholar
  51. Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool Stud 43:255–266Google Scholar
  52. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293CrossRefGoogle Scholar
  53. Vyshkvartseva NV (1975) Structure of the mandibles in the genus Calanus s.l. in relation to latitudinal zonality. In: Zvereva ZA (ed) Geographical and seasonal variability of marine plankton. Israel Program for Scientific Translations, Jerusalem, pp 186–199Google Scholar
  54. Wang RZ, Weiner S (1998) Strain-structure relations in human teeth using Moiré fringes. J Biomech 31:135–141CrossRefGoogle Scholar
  55. Weis-Fogh T (1961) Molecular interpretation of the elasticity of resilin, a rubber-like protein. J Mol Biol 3:648–667CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of Functional Morphology and BiomechanicsInstitute of Zoology, Christian-Albrechts-Universität zu KielKielGermany
  2. 2.Biological OceanographyGEOMAR Helmholtz Centre for Ocean Research KielKielGermany

Personalised recommendations