Advertisement

Marine Biology

, Volume 145, Issue 3, pp 575–583 | Cite as

Carrion-feeding on the sediment surface at nocturnal low tides by the polychaete Phyllodoce mucosa

  • C.-G. Lee
  • M. Huettel
  • J.-S. Hong
  • K. Reise
Research Article

Abstract

Harsh physical conditions in the intertidal zone are the cause of an ample amount of dead macroinvertebrates, which constitute a food source for carrion-feeders. In the European Wadden Sea, this trophic guild includes decapod crustaceans and fish when the tide is in, while during nocturnal low tides the polychaete Phyllodoce mucosa is attracted in large numbers by dead mollusks, crabs or worms on the sediment surface. Within 10 s worms emerged to the surface, crawled as far as 15 m on mucus trails towards the carcass, sucked in tissue up to one-third of their own weight, and then quickly retreated to below the surface. Abundance of P. mucosa was highest in the lower intertidal zone and winter. The seaward high abundance pattern, however, did not continue into the shallow subtidal. In summer, few were attracted during daytime or when the tide was in. However, up to 447 worms aggregated at a single crushed mussel within 20 min at dusk during low-tide exposure. This study suggests that during winter carrion-feeding is an important trophic niche on cold-temperate, intertidal mud flats occupied by a phyllodocid polychaete that is segregated in feeding time from most other scavengers and benefits from cold-sensitive benthic invertebrates.

Keywords

Sediment Surface Polychaete Tidal Flat Tidal Zone Brown Shrimp 
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.

Notes

Acknowledgements

We thank W. Armonies and N. Hernandez for helpful suggestions and reading the manuscript. Financial support was provided by Korea Science and Engineering Foundation within the framework of the KOSEF–DFG Joint Research Program 2002. The experiments comply with the current laws of the country in which the experiments were performed.

References

  1. Abele-Oeschger D, Oeschger R (1995) Enzymatic antioxidant protection in spawn, larvae and adult worms of Phyllodoce mucosa (Polychaeta). Ophelia 43:101–110Google Scholar
  2. Ahrens MJ, Hickey CW (2002) UV-photoactivation of polycyclic aromatic hydrocarbons and the sensitivity of sediment-dwelling estuarine organisms. In: UV radiation and its effects: an update 2002. Proceedings of a workshop held in Christchurch. RSNZ miscellaneous series no. 60, Royal Society of New Zealand, Wellington, pp 63–65Google Scholar
  3. Armonies W, Hellwig-Armonies M (1992) Passive settlement of Macoma balthica spat on tidal flats of the Wadden Sea and subsequent migrations of juveniles. Neth J Sea Res 29:371–378CrossRefGoogle Scholar
  4. Asmus H, Lackschewitz D, Asmus R, Scheiffarth G, Nehls G, Herrmann J-P (1998) Transporte im Nahrungsnetz eulitoraler Wattflächen des Sylt-Rømø Wattenmeeres. In: Gätje C, Reise K (eds) Ökosystem Wattenmeer—Austausch-, Transport- und Stoffumwandlungsprozesse. Springer, Berlin Heidelberg New York, pp 393–420Google Scholar
  5. Austen I (1994) The surface sediments of Königshafen variations over the past 50 years. Helgol Meeresunters 48:163–171Google Scholar
  6. Baretta JW, Ruardy P (eds) (1988) Tidal flat estuaries. Springer, Berlin Heidelberg New YorkGoogle Scholar
  7. Beukema JJ (1979) Biomass and species richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea: effects of a severe winter. Neth J Sea Res 13:203–223CrossRefGoogle Scholar
  8. Beukema JJ (1991) Changes in composition of bottom fauna of a tidal-flat area during a period of eutrophication. Mar Biol 111:293–301Google Scholar
  9. Beukema JJ (1992) Dynamics of juvenile shrimp Crangon crangon in a tidal-flat nursery of the Wadden Sea after mild and cold winters. Mar Ecol Prog Ser 83:157–165Google Scholar
  10. Beukema JJ (1993) Successive changes in distribution patterns as an adaptive strategy in the bivalve Macoma balthica (L.) in the Wadden Sea. Helgol Meeresunters 47:287–304Google Scholar
  11. Black KP, Oldman JW (1999) Wave mechanisms responsible for grain sorting and non-uniform ripple distribution across two moderate-ebergy, sandy continental shelves. Mar Geol 162:121–132CrossRefGoogle Scholar
  12. Britton JC, Morton B (1994) Marine carrion and scavengers. Oceanogr Mar Biol Annu Rev 32:369–434Google Scholar
  13. Brown AC (1961) Physiological–ecological studies on two sandy-beach Gastropoda from South Africa: Bullia digitalis Meuschen and Bullia laevissima (Gmelin). Z Morphol Oekol Tiere 49:629–657Google Scholar
  14. Brown AC (1982) The biology of sandy-beach whelks of the genus Bullia (Nassariidae). Oceanogr Mar Biol Annu Rev 20: 309–361Google Scholar
  15. Cohen JE (1978) Food webs and niche space. Princeton University Press, PrincetonGoogle Scholar
  16. Creutzberg F, Fonds M (1971) The seasonal variation in the distribution of some demersal fish species in the Dutch Wadden Sea. Thalassia Jugosl 7:13–23Google Scholar
  17. Crisp DJ (ed) (1964) The effects of the severe winter of 1962–63 on marine life in Britain. J Anim Ecol 33:165–210Google Scholar
  18. Eriksson S, Tallmark B (1974) The influence of environmental factors on the diurnal rhythm of the prosobranch gastropod Nassarius reticulatus (L.) from a non-tidal area. Zoon 2:135–142Google Scholar
  19. Eriksson S, Evans S, Tallmark B (1975a) On the coexistence of scavengers on shallow, sandy bottoms in Gullmar Fjord (Sweden): adaptations to substratum, temperature, and salinity. Zoon 3:65–70Google Scholar
  20. Eriksson S, Evans S, Tallmark B (1975b) On the coexistence of scavengers on shallow, sandy bottoms in Gullmar Fjord (Sweden): activity patterns and feeding activity. Zoon 3:121–124Google Scholar
  21. Farke H, Wilde PAWJ de, Berghuis EM (1979) Distribution of juvenile and adult Arenicola marina on a tidal mud flat and the importance of nearshore areas for recruitment. Neth J Sea Res 13:354–361CrossRefGoogle Scholar
  22. Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Annu Rev 17:193–284Google Scholar
  23. Fenske C (1997) The importance of intraspecific competition in a Littorina littorea population in the Wadden Sea. Hydrobiologia 355:29–39CrossRefGoogle Scholar
  24. Gillandt L (1979) Zur Systematik, Autökologie und Biologie der Polychaeten des Helgoländer Felslitorals. Mitt Hambg Zool Mus Inst 76:19–73Google Scholar
  25. Gravier C (1896) Recherches sur les phyllodociens. Bull Sci Fr Belg 294Google Scholar
  26. Halliwell B, Gutteridge JMC (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501–514PubMedGoogle Scholar
  27. Hartmann-Schröder G (1996) Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands,vol 58. Fischer, JenaGoogle Scholar
  28. Hauser RN (1973) Bestandsänderungen der Macrofauna an einer Station im ostfriesischen Watt. Jahresber Forschstn Norderney 24:171–203Google Scholar
  29. Hayes FR (1929) Contributions to the study of marine gastropods. III. Development, growth and behaviour of Littorina. Contrib Can Biol Fish 4:415–430Google Scholar
  30. Hayward PJ, Ryland JS (1990) The marine fauna of the British Isles and North-West Europe. Oxford University Press, New YorkGoogle Scholar
  31. Hurd LE (1985) On the importance of carrion to reproduction in an omnivorous estuarine neogastropod, Ilyanassa obsoleta (Say). Oecologia 65:513–515Google Scholar
  32. Klein-Breteler WCM (1976) Migration of the shore crab, Carcinus maenas, in the Dutch Wadden Sea. Neth J Sea Res 10:338–353CrossRefGoogle Scholar
  33. Kuipers BR, Wilde PAWJ, Creutzberg F (1981) Energy flow in a tidal flat ecosystem. Mar Ecol Prog Ser 5:215–221Google Scholar
  34. McKillup SC, McKillup RV (1997) Effect of food supplementation on the growth of an intertidal scavenger. Mar Ecol Prog Ser 148:109–114Google Scholar
  35. Michaelis H (1987) Bestandsaufnahme des eulitoralen Makrobenthos im Jadebusen in Verbindung mit einer Luftbild-Analyse. Jahresber Forschstn Norderney 38:13–97Google Scholar
  36. Miron GY, Desrosiers GL (1990) Distributions and population structures of two intertidal estuarine polychaetes in the lower St. Lawrence Estuary, with special reference to enviromental factors. Mar Biol 105: 297–306Google Scholar
  37. Morton B, Chan K (1999) Hunger rapidly overrides the risk of predation in the subtidal scavenger Nassarius siquijorensis (Gastropoda: Nassariidae): an energy budget and a comparison with the intertidal Nassarius festivus in Hong Kong. J Exp Mar Biol Ecol 240:213–228CrossRefGoogle Scholar
  38. Petraitis PS (2002) Effects of intraspecific competition and scavenging on growth of the periwinkle Littorina littorea. Mar Ecol Prog Ser 236:179–187Google Scholar
  39. Pleijel F (1988) Phyllodoce (Polychaeta, Phyllodocidae) from northern Europe. Zool Scr 17:141–153Google Scholar
  40. Reichert A, Dörjes J (1980) Die Bodenfauna des Crildumersieler Wattes (Jade, Nordsee) und ihre Veränderung nach dem Eiswinter 1978/79. Senckenb Marit 12:213–245Google Scholar
  41. Reise K (1978) Experiments on epibenthic predation in the Wadden Sea. Helgol Wiss Meeresunters 31:55–101Google Scholar
  42. Reise K (1979a) Spatial configurations generated by motile benthic polychaetes. Helgol Wiss Meeresunters 32:55–72Google Scholar
  43. Reise K (1979b) Moderate predation on meiofauna by the macrobenthos of the Wadden Sea. Helgol Wiss Meeresunters 32:453–465Google Scholar
  44. Reise K (1982) Long-term changes in the macrobenthic invertebrate fauna of the Wadden Sea: are polychaetes about to take over? Neth J Sea Res 16:29–36CrossRefGoogle Scholar
  45. Reise K (1985) Tidal flat ecology. Ecological studies, vol 54. Springer, Berlin Heidelberg New YorkGoogle Scholar
  46. Reise K, Herre E, Sturm M (1994) Biomass and abundance of macrofauna in intertidal sediments of Königshafen in the northern Wadden Sea. Helgol Meeresunters 48:201–215Google Scholar
  47. Reise K, Simon M, Herre E (2001) Density dependant recruitment after winter disturbance on tidal flats by the lugworm Arenicola marina. Helgol Mar Res 55:161–165CrossRefGoogle Scholar
  48. Sach G (1975) Zur Fortpflanzung des Polychaeten Anaitides mucosa. Mar Biol 31:157–160Google Scholar
  49. Sach G (1977) Zur Fortpflanzung, Histogenese der Geschlechtszellen, Eireifung und frühen Larvalentwicklung von Anaitides mucosa (Polychaeta, Phyllodocidae). Diplomarbeit, Universität Kiel, Kiel, GermanyGoogle Scholar
  50. Smidt ELB (1951) Animal production in the Danish Wadden Sea. Medd Dan Fisk- Havunders1–151Google Scholar
  51. Strasser M, Pieloth U (2001) Recolonization pattern of the polychaete Lanice conchilega on an intertidal sand flat following the severe winter of 1995/96. Helgol Mar Res 55:176–181CrossRefGoogle Scholar
  52. Strasser M, Reinwald T, Reise K (2001) Differential effects of the severe winter of 1995/96 on the intertidal bivalves Mytilus edulis, Cerastoderma edule and Mya arenaria in the northern Wadden Sea. Helgol Mar Res 55:190–197CrossRefGoogle Scholar
  53. Szymczak R, Waite TD (1988) Generation and decay of hydrogen peroxide in estuarine waters. Aust J Mar Freshw Res 39:298–299Google Scholar
  54. Tallmark B (1980) Population dynamics of Nassarius reticulatus (Gastropoda, Prosobranchia) in Gullmar Fjord, Sweden. Mar Ecol Prog Ser 3:51–62Google Scholar
  55. Thiel M, Reise K (1993) Interaction of nemertines and their prey on tidal flats. Neth J Sea Res 31:163–172CrossRefGoogle Scholar
  56. Thiel M, Nordhausen W, Reise K (1996) Nocturnal surface activity of endobenthic nemertines on tidal flats. In: Eleftheriou A, et al (eds) Biology and ecology of shallow coastal waters. Olsen and Olsen, Fredensborg, Denmark, pp 283–289Google Scholar
  57. Wohlenberg E (1937) Die Wattenmeer-Lebensgemeinschaften im Königshafen von Sylt. Helgol Wiss Meeresunters 1:1–92Google Scholar
  58. Yonge CM (1976) Neogastropods—scavengers and predators. In: Yonge CM, Thompson TE (eds) Living marine molluscs. Collins, London, pp 97–108Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of OceanographyInha UniversityIncheonKorea
  2. 2.Department of OceanographyFlorida State UniversityTallahasseeUSA
  3. 3.Wadden Sea Station SyltAlfred Wegener Institute for Polar and Marine ResearchListGermany

Personalised recommendations