Marine Biology

, Volume 144, Issue 6, pp 1151–1155 | Cite as

Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda)

Research Article

Abstract

The mutualism between the Hawaiian bobtail squid Euprymna scolopes and the luminescent symbiont Vibrio fischeri has been used extensively as a model system for studies ranging from co-speciation and biogeography to gene regulation and the evolution of pathogenesis. In this association, the luminescent bacterium V. fischeri is housed in a complex light organ within the mantle cavity of E. scolopes. Prior hypotheses have assumed that sepiolid squids in general utilize the bioluminescence produced by their V. fischeri symbionts for counterillumination, a behavior that helps squid camouflage themselves by matching down-welling moonlight via silhouette reduction. This assumption, based solely on the morphology of the squid light organ, has never been empirically tested for Euprymna in the laboratory. Here, we present data demonstrating that E. scolopes can modify the intensity of light produced by V. fischeri in the light organ as down-welling light intensity changes. Bacterial bioluminescence from the light organ is directly correlated with down-welling light intensity, suggesting that E. scolopes individuals utilize and control V. fischeri luminescence for counterillumination.

References

  1. Boettcher KJ, Ruby EG, McFall-Ngai MJ (1996) Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol B 179:65–73Google Scholar
  2. Harper RD, Case JF (1999) Counterillumination and its anti-predatory value in the plainfin midshipman fish Porichthys notatus. Mar Biol 134:529–540CrossRefGoogle Scholar
  3. Hartline DK, Buskey EJ, Lenz PH (1999) Rapid jumps and bioluminescence elicited by controlled hydrodynamic stimuli in a mesopelagic copepod, Pleuromamma xiphias. Biol Bull 197:132–143Google Scholar
  4. Hastings JW, Makemson JC, Dunlap PV (1987) How are growth and luminescence regulated independently in light organ symbionts? Symbiosis 4:3–24Google Scholar
  5. Herring PJ (2000) Species abundance, sexual encounter and bioluminescent signaling in the deep sea. Philos Trans R Soc Lond B 355:1273–1276CrossRefGoogle Scholar
  6. Johnson S, Balser EJ, Fisher EC, Widder EA (1999) Bioluminescence in the deep-sea cirrate octopod Stauroteuthis syrtensis Verrill (Mollusca: Cephalopoda). Biol Bull 197:26–39Google Scholar
  7. Lindsay SM, Frank TM, Kent J, Partridge JC, Latz MI (1999) Spectral sensitivity of vision and bioluminescence in the midwater shrimp, Sergestes similis. Biol Bull 197:348–360PubMedGoogle Scholar
  8. Mangold K, Boletzky S (1988) Mediterranean cephalopod fauna. In: Clarke MR, Trueman ER (eds) The Mollusca. Academic Press, San Diego, Calif., pp 315–330Google Scholar
  9. McFall-Ngai MJ (1989) Luminous bacterial symbiosis in fish evolution: adaptive radiation among the Leiognathid fishes. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge, Mass., pp 381–409Google Scholar
  10. McFall-Ngai MJ (1990) Crypsis in the pelagic environment. Am Zool 30:175–188Google Scholar
  11. McFall-Ngai MJ (1999) Consequences of evolving with bacterial symbionts: lessons from the squid-vibrio association. Annu Rev Ecol Syst 30:235–256Google Scholar
  12. McFall-Ngai MJ, Montgomery MK (1990) The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes Berry (Cephalopoda: Sepiolidae). Biol Bull 179:332–339Google Scholar
  13. McFall-Ngai MJ, Ruby EG (1991) Symbiont recognition and subsequent morphogenesis as early events in an animal–bacterial symbiosis. Science 254:1491–1494PubMedGoogle Scholar
  14. McNulty JA, Nafpaktitis BG (1976) The structure and development of the pineal complex in the lanternfish Triphoturus mexicanus (family Myctophidae). J Morphol 150:579–605PubMedGoogle Scholar
  15. Montgomery MK, McFall-Ngai MJ (1992) The muscle-derived lens of a squid bioluminescent organ is biochemically convergent with the ocular lens. Evidence for recruitment of aldehyde dehydrogenase as a predominant structural protein. J Biol Chem 267:20999–21003PubMedGoogle Scholar
  16. Montgomery MK, McFall-Ngai M (1993) Embryonic development of the light organ of the Sepiolid squid Euprymna scolopes Berry. Biol Bull 184:296–308Google Scholar
  17. Montgomery MK, McFall-Ngai MJ (1994) Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Eupyrmna scolopes. Development 120:1719–1729PubMedGoogle Scholar
  18. Munk O (1999) The escal photophore of ceratioids (Pisces: Ceratioidei): a review of structure and function. Acta Zool (Stockholm) 80:265–284Google Scholar
  19. Nealson KH, Hastings JW (1991) The luminous bacteria. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The Prokaryotes, a handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. Springer, Berlin Heidelberg New York, pp 625–639Google Scholar
  20. Nesis KN (1982) Cephalopods of the world. TFH Publications, Neptune City, N.J.Google Scholar
  21. Nishiguchi MK (2001) Co-evolution of symbionts and hosts: The sepiolid-Vibrio model. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Cole-Kluwer Academic, Dordrecht, The Netherlands, pp 757–774Google Scholar
  22. Nishiguchi MK (2002) Host-symbiont recognition in the environmentally transmitted sepiolid squid-Vibrio mutualism. Microb Ecol 44:10–18PubMedGoogle Scholar
  23. Nishiguchi MK, Lamarcq LH, Ruby EG, McFall-Ngai MJ (1996) Competitive dominance of native strain symbiotic bacteria measured by colonization and in situ hybridization. Am Zool 36:41AGoogle Scholar
  24. Nishiguchi MK, Ruby EG, McFall-Ngai MJ (1998) Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid-vibrio symbioses. Appl Environ Microbiol 64:3209–3213PubMedGoogle Scholar
  25. Nyholm SV, McFall-Ngai MJ (1998) Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol Bull 195:89–97PubMedGoogle Scholar
  26. Parry M (2000) A description of the nuchal organ, a possible photoreceptor, in Euprymna scolopes and other cephalopods. J Zool (Lond) 252:163–177Google Scholar
  27. Ruby EG (1996) Lessons from a cooperative, bacterial-animal association: the Vibrio fischeriEuprymna scolopes light organ symbiosis. Annu Rev Microbiol 50:591–624CrossRefPubMedGoogle Scholar
  28. Ruby EG (1999) Ecology of a benign “infection”: colonization of the squid luminous organ by Vibrio fischeri. American Society of Microbiology, Washington, D.C.Google Scholar
  29. Ruby EG, Asato LM (1993) Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159:160–167PubMedGoogle Scholar
  30. Ruby EG, McFall-Ngai MJ (1999) Oxygen-utilizing reactions and symbiotic colonization of the squid light organ by Vibrio fischeri. Trends Microbiol 7:414–420CrossRefPubMedGoogle Scholar
  31. Ruby EG, Nealson KH (1976) Symbiotic associations of Photobacterium fischeri with the marine luminous fish Monocentris japonica: a model of symbiosis based on bacterial studies. Biol Bull 151:574–586PubMedGoogle Scholar
  32. Small AL, McFall-Ngai MJ (1998) A halide peroxidase in tissues interacting with bacteria in the squids Euprymna scolopes. J Cell Biochem 72:445–457CrossRefGoogle Scholar
  33. Visick KL, Foster JS, Doino JA, McFall-Ngai MJ, Ruby EG (2000) Vibrio fischeri lux genes play and important role in colonization and development of the host light organ. J Bacteriol 182:4578–4586CrossRefPubMedGoogle Scholar
  34. Young RE (1977) Ventral bioluminescent countershading in midwater cephalopods. Symp Zool Soc Lond 38:161–190Google Scholar
  35. Young RE, Roper CFE (1976) Bioluminescent countershading in mid-water animals: evidence from living squid. Science 191:1046–1048PubMedGoogle Scholar
  36. Young RE, Roper CFE (1977) Intensity regulation of bioluminescence during countershading in living midwater animals. Fish Bull U S:239–252Google Scholar
  37. Young RE, Roper CFE, Walters JF (1979) Eyes and extraocular photoreceptors in midwater cephalopods and fishes: their roles in detecting down-welling light for counterillumination. Mar Biol 51:371–380Google Scholar
  38. Young RE, Kampa EM, Maynard SD, Mencher FM, Roper CFE (1980) Counterillumination and the upper depth limits of midwater animals. Deep-Sea Res 27A:671–691Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of BiologyNew Mexico State University Las CrucesUSA

Personalised recommendations