Advertisement

Predator-induced vertical behavior of a ctenophore

  • Josefin TitelmanEmail author
  • Lars Johan Hansson
  • Trygve Nilsen
  • Sean P. Colin
  • John H. Costello
JELLYFISH BLOOMS
  • 660 Downloads
Part of the Developments in Hydrobiology book series (DIHY, volume 220)

Abstract

Although many studies have focused on Mnemiopsis leidyi predation, little is known about the role of this ctenophore as prey when abundant in native and invaded pelagic systems. We examined the response of the ctenophore M. leidyi to the predatory ctenophore Beroe ovata in an experiment in which the two species could potentially sense each other while being physically separated. On average, M. leidyi responded to the predator’s presence by increasing variability in swimming speeds and by lowering their vertical distribution. Such behavior may help explain field records of vertical migration, as well as stratified and near-bottom distributions of M. leidyi.

Keywords

Beroe spp. Mnemiopsis leidyi Ctenophore Behavior Vertical distribution Predator–prey 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgments

We thank J. E. Skjæraasen, P. Tiselius, E. Selander, T. Andersen, and reviewers for constructive comments. This is a contribution to Baltic Zooplankton Cascades (BAZOOCA) program funded by Baltic Organizations Network for funding Science, European Economic Interest Grouping (BONUS EEIG). We received financial support from Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS), Sweden (grant numbers 2007-1105 to LJH and JT; 2006-1054 and 2008-1586 to JT), the National Science Foundation, USA (grant numbers OCE-0350834 and OCE-0623508 to JHC; OCE-0351398 and OCE-0623534 to SPC.), Stiftelsen Konung Carl XVI Gustafs 50-årsfond för vetenskap, teknik och miljö (to JT), and Birgit och Birger Wåhlströms minnesfond (to JT).

References

  1. Albert, D. J., 2011. What’s on the mind of a jellyfish? A review of behavioural observations on Aurelia sp. jellyfish. Neuroscience and Biobehavioral Reviews 35: 474–482.PubMedCrossRefGoogle Scholar
  2. Aronova, M. Z. & T. M. Alekseeva, 2002. Second messengers in the locomotor–sensory system of first multicellulars. The IP3-containing compartments in chemoreceptor cells of the comb jelly Beroe cucumis from data of cytochemical study. Journal of Evolutionary Biochemistry and Physiology 38: 318–329.CrossRefGoogle Scholar
  3. Aronova, M. Z. & T. M. Alekseeva, 2003. Development of chemoreceptor cells in oral epithelium of adult jelly-fish Beroe cucumis. Journal of Evolutionary Biochemistry and Physiology 39: 714–723.CrossRefGoogle Scholar
  4. Cohen, J. H. & R. B. Forward Jr., 2003. Ctenophore kairomones and modified aminosugar disaccharides alter the shadow response in a larval crab. Journal of Plankton Research 25: 203–213.CrossRefGoogle Scholar
  5. Colin, S. P., J. H. Costello, L. J. Hansson, J. Titelman & J. O. Dabiri, 2010. Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi. Proceedings of the National Academy of Sciences of the United States of America 107: 17223–17227.PubMedCrossRefGoogle Scholar
  6. Condon, R. H. & D. K. Steinberg, 2008. Development, biological regulation, and fate of ctenophore blooms in the York River estuary, Chesapeake Bay. Marine Ecology Progress Series 369: 153–168.CrossRefGoogle Scholar
  7. Costello, J. H., K. M. Bayha, H. W. Mianzan, T. A. Shiganova & J. E. Purcell, 2012. Transitions of Mnemiopsis leidyi (Ctenophora: Lobata) 3 from a native to an exotic species: a review. Hydrobiologia. doi: 10.1007/s10750-012-1037-9.
  8. Costello, J. H. & H. W. Mianzan, 2003. Sampling field distributions of Mnemiopsis leidyi (Ctenophora, Lobata): planktonic or benthic methods? Journal of Plankton Research 25: 455–459.CrossRefGoogle Scholar
  9. Costello, J. H., B. K. Sullivan, D. J. Gifford, D. Van Keuren & L. J. Sullivan, 2006. Seasonal refugia, shoreward thermal amplification, and metapopulation dynamics of the ctenophore Mnemiopsis leidyi in Narragansett Bay, Rhode Island. Limnology and Oceanography 51: 1819–1831.CrossRefGoogle Scholar
  10. Decker, M. B., D. L. Breitburg & J. E. Purcell, 2004. Effects of low dissolved oxygen on zooplankton predation by the ctenophore, Mnemiopsis leidyi. Marine Ecology Progress Series 280: 163–172.CrossRefGoogle Scholar
  11. Esser, M., W. Greve & M. Boersma, 2004. Effects of temperature and the presence of benthic predators on the vertical distribution of the ctenophore Pleurobrachia pileus. Marine Biology 145: 595–601.CrossRefGoogle Scholar
  12. Falkenhaug, T., 1996. Distributional and seasonal patterns of ctenophores in Malangen, northern Norway. Marine Ecology Progress Series 140: 59–70.CrossRefGoogle Scholar
  13. Falkenhaug, T. & O. B. Stabell, 1996. Chemical ecology of predator–prey interactions in ctenophores. Marine and Freshwater Behavior and Physiology 27: 249–260.CrossRefGoogle Scholar
  14. Fuentes, V. L., D. L. Angel, K. M. Bayha, D. Atienza, D. Edelist, C. Bordehore, J. M. Gili & J. E. Purcell, 2010. Blooms of the invasive ctenophore, Mnemiopsis leidyi, span the Mediterranean Sea in 2009. Hydrobiologia 645: 23–37.CrossRefGoogle Scholar
  15. Greve, W. & F. Reiners, 1988. Plankton time–space dynamics in German Bight—a systems-approach. Oecologia 77: 487–496.CrossRefGoogle Scholar
  16. Hansson, L. J. & B. Norrman, 1995. Release of dissolved organic carbon (DOC) by the scyphozoan jellyfish Aurelia aurita and its potential influence on the production of planktic bacteria. Marine Biology 121: 527–532.CrossRefGoogle Scholar
  17. Harbison, G. R., L. P. Madin & N. R. Swanberg, 1978. On the natural history and distribution of oceanic ctenophores. Deep Sea Research 25: 233–256.CrossRefGoogle Scholar
  18. Hays, G. C., 2003. A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503: 163–170.CrossRefGoogle Scholar
  19. Horridge, G. A., 1965. Non-motile sensory cilia and neuromuscular junctions in a ctenophore independent effector organ. Proceedings of the Royal Society B 162: 333–350.CrossRefGoogle Scholar
  20. Hosia, A. & J. Titelman, 2011. Intraguild predation between the native North Sea jellyfish Cyanea capillata and the invasive ctenophore Mnemiopsis leidyi. Journal of Plankton Research 33: 535–540.CrossRefGoogle Scholar
  21. Hosia, A., J. Titelman, L. J. Hansson & M. Haraldsson, 2011. Interactions between native and alien ctenophores: Beroe gracilis and Mnemiopsis leidyi in Gullmarsfjorden. Marine Ecology Progress Series 422: 129–138.CrossRefGoogle Scholar
  22. Jaspers, C., J. Titelman, L. J. Hansson, M. Haraldsson & C. Ditlefsen, 2011. The invasive ctenophore Mnemiopsis leidyi poses no direct threat to Baltic cod eggs and larvae. Limnology and Oceanography 56: 431–439.Google Scholar
  23. Javidpour, J., J. Molinero, J. Peschutter & U. Sommer, 2009. Seasonal changes and population dynamics of the ctenophore Mnemiopsis leidyi after its first year of invasion in the Kiel Fjord, Western Baltic Sea. Biological Invasions 11: 873–882.CrossRefGoogle Scholar
  24. Kass-Simon, G. & L. A. Hufnagel, 1992. Suspected chemoreceptors in coelenterates and ctenophores. Microscopy Research and Technique 22: 265–284.PubMedCrossRefGoogle Scholar
  25. Kreps, T. A., J. E. Purcell & K. B. Heidelberg, 1997. Escape of the ctenophore Mnemiopsis leidyi from the scyphomedusa predator Chrysaora quinquecirrha. Marine Biology 128: 441–446.CrossRefGoogle Scholar
  26. McKelvey, L. M. & R. B. Forward Jr, 1995. Activation of brine shrimp nauplii, photoresponses involved in diel vertical migration by chemical cues from visual and non-visual planktivores. Journal of Plankton Research 17: 2191–2206.CrossRefGoogle Scholar
  27. Mianzan, H. W., P. M. Martos, J. H. Costello & R. A. Guerro, 2010. Avoidance of hydrodynamically mixed environments by Mnemiopsis leidyi (Ctenophora: Lobata) in open-sea populations from Patagonia, Argentina. Hydrobiologia 645: 113–124.CrossRefGoogle Scholar
  28. Miller, R. J., 1974. Distribution and biomass of an estuarine ctenophore population, Mnemiopsis leidyi (A. Agassiz). Chesapeake Science 15: 1–8.CrossRefGoogle Scholar
  29. Moss, A. G., B. Wells & L. Muellner, 2004. A mechanosensory system that controls feeding in adult Mnemiopsis. Hydrobiologia 530–531: 145–153.CrossRefGoogle Scholar
  30. Ohman, M. D., 1988. Behavioral responses of zooplankton to predation. Bulletin of Marine Science 43: 530–550.Google Scholar
  31. Oviatt, C. A. & P. M. Kremer, 1977. Predation on the ctenophore, Mnemiopsis leidyi, by butterfish, Periplus triacanthus, in Narragansett Bay, Rhode Island. Chesapeake Science 18: 236–240.CrossRefGoogle Scholar
  32. Pinheiro, J., S. DebRoy, D. Sarkar & The R Core team, 2008. nlme: linear and nonlinear mixed effects models. R package version 3.1-89.Google Scholar
  33. Pitt, K. A., D. T. Welsh & R. H. Condon, 2009. Influence of jellyfish blooms on carbon, nitrogen and phosphorous cycling and plankton production. Hydrobiologia 616: 133–149.CrossRefGoogle Scholar
  34. Purcell, J. E., 1991. A review of cnidarians and ctenophores feeding on competitors in the plankton. Hydrobiologia 216–217: 335–342.CrossRefGoogle Scholar
  35. Purcell, J. E. & J. H. Cowan, 1995. Predation by the scyphomedusan Chrysaora quinquecirrha on Mnemiopsis leidyi ctenophores. Marine Ecology Progress Series 129: 63–70.CrossRefGoogle Scholar
  36. Purcell, J. E., T. A. Shiganova, M. B. Decker & E. D. Houde, 2001. The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin. Hydrobiologia 451: 145–176.CrossRefGoogle Scholar
  37. R Development Core Team, 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0 [available on internet at http://www.R-project.org].
  38. Rasband, W. S., 2008. Image J. U. S. National Institutes of Health, Bethesda, MD [available on internet at http://imagej.nih.gov/ij/, 1997–2011]. Accessed 23.08.2008.
  39. Riemann, L., J. Titelman & U. Båmstedt, 2006. Links between jellyfish and microbes in a jellyfish dominated fjord. Marine Ecology Progress Series 325: 29–42.CrossRefGoogle Scholar
  40. Riisgård, H. U., L. Bøttiger, C. V. Madsen & J. E. Purcell, 2007. Invasive ctenophore Mnemiopsis leidyi in Limfjorden (Denmark) in late summer 2007—assessment of abundance and predation effects. Aquatic Invasions 2: 395–401.CrossRefGoogle Scholar
  41. Stone, R., 2005. Attack of the killer jellies. Science 309: 1805–1806.PubMedCrossRefGoogle Scholar
  42. Swanberg, N., 1974. The feeding behavior of Beroe ovata. Marine Biology 24: 69–76.CrossRefGoogle Scholar
  43. Thuesen, E. V., L. D. Rutherford & P. L. Brommer, 2005. The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi. Journal of Marine Biological Association of the United Kingdom 85: 627–633.CrossRefGoogle Scholar
  44. Titelman, J. & Ø. Fiksen, 2004. Ontogenetic vertical distribution patterns in small copepods: field observations and model predictions. Marine Ecology Progress Series 284: 49–63.CrossRefGoogle Scholar
  45. Titelman, J., L. Gandon, A. Goarant & T. Nilsen, 2007. Intraguild predatory interactions between the jellyfish Cyanea capillata and Aurelia aurita. Marine Biology 152: 745–756.CrossRefGoogle Scholar
  46. Titelman, J., L. Riemann, T. A. Sørnes, T. Nilsen, P. Griekspoor & U. Båmstedt, 2006. Turnover of dead jellyfish: stimulation and retardation of microbial activity. Marine Ecology Progress Series 325: 43–58.CrossRefGoogle Scholar
  47. Vinogradov, M. E., E. A. Shushkina & T. A. Lukasheva, 2005. Population dynamics of the ctenophores Mnemiopsis leidyi and Beroe ovata as a predator–prey system in the near-shore communities of the Black Sea. Oceanology 45(Suppl 1): S161–S167.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Josefin Titelman
    • 1
    Email author
  • Lars Johan Hansson
    • 2
  • Trygve Nilsen
    • 3
  • Sean P. Colin
    • 4
  • John H. Costello
    • 5
  1. 1.Department of BiologyUniversity of OsloOsloNorway
  2. 2.Department of Marine Ecology-GöteborgUniversity of GothenburgGöteborgSweden
  3. 3.Department of MathematicsUniversity of BergenBergenNorway
  4. 4.Environmental Sciences and Marine BiologyRoger Williams UniversityBristolUSA
  5. 5.Biology DepartmentProvidence CollegeProvidenceUSA

Personalised recommendations