Skip to main content
Log in

Three digestive movements in Hydra regulated by the diffuse nerve net in the body column

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The mammalian digestive tract undergoes various digestive movements such as peristalsis and segmentation movement. How those digestive movements and the underlying mechanisms appeared in evolution remains unraveled. A widely accepted view has been that, early in evolution, the digestive process was static based upon diffusion, and later it became dynamic involving digestive movements. Here, we report digestive movements which occur in Hydra, a member of the phylum Cnidaria. We find that the body column of Hydra undergoes a series of movements when fed with Artemia. Comparison of the movements to those in mammals showed similarities in appearance to esophageal reflex, segmentation movement, and defecation reflex. When nerve cells were eliminated, polyps showed only a weak segmentation movement, demonstrating that the diffuse nerve net in the body column of Hydra primarily regulates the movements just as the netlike enteric nervous system does in mammals. Elimination of both secretory gland cells and nerve cells resulted in the complete loss of movement, suggesting that the gland cells are involved in the weak movement. Overall, these observations suggest that the digestive process in Hydra is dynamic and that the diffuse nerve net regulates the digestive movements as a primitive form of enteric nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A, B
Fig. 2A–C
Fig. 3
Fig. 4A, B
Fig. 5

Similar content being viewed by others

References

  • Bridge D, Cunningham CW, Schierwater B, DeSalle R, Buss LW (1992) Class-level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. Proc Natl Acad Sci USA 89:8750–8753

    CAS  PubMed  Google Scholar 

  • Brookes SJH (2001) Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 262:58–70

    Article  CAS  PubMed  Google Scholar 

  • Campbell RD (1976) Elimination of Hydra interstitial and nerve cells by means of colchicine. J Cell Sci 21:1–13

    CAS  PubMed  Google Scholar 

  • Cannon WB (1912) Peristalsis, segmentation and the myenteric reflex. Am J Physiol 30:114–128

    Google Scholar 

  • David CN (1973) A quantitative method for maceration of Hydra tissue. Wilhelm Roux’s Arch Entw Mech Org 171:259–268

  • Dogiel AS (1899) Über den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugethiere. Arch Anat Physiol Leipzig, Anat Abt 1899:130–158

  • Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193

    CAS  PubMed  Google Scholar 

  • Gabella G (1994) In: Johnson LR (ed) Physiology of the gastrointestinal tract, 3rd edn. Raven Press, New York, pp 753–754

  • Gershon MD, Erde SM (1981) The nervous system of the gut. Gastroenterology 80:1571–1594

    CAS  PubMed  Google Scholar 

  • Goyal RK, Padmanabhan R, Sang Q (2001) Neural circuits in swallowing and abdominal vagal afferent-mediated lower esophageal sphincter relaxation. Am J Med 111(Suppl):95S-105S

    Article  PubMed  Google Scholar 

  • Hiatt RB, Goodman I, Overweg NI (1970) Serotonin and intestinal motility. Am J Surg 119:527–529

    CAS  PubMed  Google Scholar 

  • Hukuhara T, Yamagami M, Nakayama S (1958) On the intestinal intrinsic reflexes. Jpn J Physiol 8:9–20

    CAS  PubMed  Google Scholar 

  • Hukuhara T, Sumi T, Kotani S (1961a) The role of the ganglion cells in the small intestine taken in the intestinal intrinsic reflex. Jpn J Physiol 11:281–288

    CAS  Google Scholar 

  • Hukuhara T, Kotani S, Sato G (1961b) Effects of destruction of intramural ganglion cells on colonic motility: possible genesis of congenital megacolon. Jpn J Physiol 11:635–640

    CAS  PubMed  Google Scholar 

  • Koizumi O, Itazawa M, Mizumoto H, Minobe S, Javois LC, Grimmelikhuijzen CJ, Bode HR (1992) Nerve ring of the hypostome in Hydra. I. Its structure, development, and maintenance. J Comp Neurol 326:7–21

    CAS  PubMed  Google Scholar 

  • Lentz TL (1966) The cell biology of Hydra. North-Holland Publishing, Amsterdam, pp 61–67

  • Matthews GG (1997) Neurobiology: molecules, cells, and systems. Blackwell, Cambridge, pp 23–24

  • Morishita F, Nitagai Y, Furukawa Y, Matsushima O, Takahashi T, Hatta M Fujisawa T, Tunamoto S, Koizumi O (2003) Identification of a vasopressin-like immunoreactive substance in Hydra. Peptides 2003:17–26

    Article  Google Scholar 

  • Mueller JF (1950) Some observations on the structure of Hydra, with particular reference to the muscular system. Trans Am Microsc Soc 96:133–147

    Google Scholar 

  • Murate M, Takahashi-Iwanaga H, Kurosaki R, Takada M, Koizumi O (1996) Scanning electron microscopy of endodermal sensory cells of Hydra magnipapillata. Cell Tissue Res 283:455–459

    Google Scholar 

  • Nishimiya-Fujisawa C, Sugiyama T (1993) Genetic analysis of developmental mechanisms in Hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata. Dev Biol 157:1-9

    Article  CAS  Google Scholar 

  • Price WE, Shehadeh Z, Thompson GH, Underwood LD, Jacobson ED (1969) Effects of acetylcholine on intestinal blood flow and motility. Am J Physiol 216:343–347

    CAS  PubMed  Google Scholar 

  • Ruppert EE, Barnes RD (1994) Invertebrate zoology, 6th edn. Saunders College Publishing, Philadelphia

  • Sakaguchi M, Mizusina A, Kobayakawa Y (1996) Structure, development, and maintenance of the nerve net of the body column in Hydra. J Comp Neurol 373:41–54

    Article  CAS  PubMed  Google Scholar 

  • Sanders KM, Ordog T, Koh SD, Torihashi S, Ward SM (1999) Development and plasticity of interstitial cells of Cajal. Neurogastroenterol Motil 11:311–338

    CAS  PubMed  Google Scholar 

  • Shimizu H (2002) Feeding and wounding responses in Hydra suggest functional and structural polarization of the tentacle nervous system. Comp Biochem Physiol A Mol Integr Physiol 131:669–674

    Article  CAS  PubMed  Google Scholar 

  • Shimizu H, Fujisawa T (2003) Peduncle of Hydra and the heart of higher organisms share a common ancestral origin. Genesis 36:182–186

    Article  CAS  Google Scholar 

  • Sugiyama T, Fujisawa T (1977) Genetic analysis of developmental mechanisms in Hydra. I. Sexual reproduction of Hydra magnipapillata and isolation of mutants. Dev Growth Differ 19:187–200

    Google Scholar 

  • Sugiyama T, Fujisawa T (1978) Genetic analysis of developmental mechanisms in Hydra. V. Cell lineage and development of chimera Hydra. J Cell Sci 32:215–232

    CAS  PubMed  Google Scholar 

  • Swenson O (2002) Hirschsprung’s disease: a review. Pediatrics 109:914–918

    PubMed  Google Scholar 

  • Takaki M, Neya T, Nakayama S (1987) Functional role of lumbar sympathetic nerves and supraspinal mechanism in the defecation reflex of the cat. Acta Med Okayama 41:249–257

    CAS  PubMed  Google Scholar 

  • Takano J, Sugiyama T (1983) Genetic analysis of developmental mechanisms in Hydra. VIII. Head-activation and head-inhibition potentials of a slow-budding strain (L4). J Embryol Exp Morphol 78:141–168

    CAS  PubMed  Google Scholar 

  • Trendelenburg P (1917) Physiologische und pharmakologische Versuche über die Dünndarm Peristaltik. Naunyn-Schmiedeberg’s Arch Exp Pathol Pharmakol 81:55–129

  • Trueman ER, Ansell AD (1969) The mechanisms of burrowing into soft substrata by marine animals. Oceanogr Mar Biol Annu Rev 7:315–366

    Google Scholar 

  • Westfall JA (1996) Ultrastructure of synapses in the first-evolved nervous systems. J Neurocytol 25:735–746

    CAS  Google Scholar 

  • Westfall JA, Yamataka S, Enos PD (1971) Ultrastructural evidence of polarized synapses in the nerve net of Hydra. J Cell Biol 51:318–323

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. M. Takaki at Nara Medical University for fruitful discussions, a number of valuable suggestions, and providing video images of digestive movements. We also thank Prof. A. Kuwahara and Dr. Karaki at Shizuoka Prefectural University for critical reading of the manuscript. This work was supported in part by grants from the Japanese Ministry of Education, Culture, Sports, Science and Technology of Japan, and the Japan Space Forum (Ground Research Announcement for Space Utilization) to T.F.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroshi Shimizu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shimizu, H., Koizumi, O. & Fujisawa, T. Three digestive movements in Hydra regulated by the diffuse nerve net in the body column. J Comp Physiol A 190, 623–630 (2004). https://doi.org/10.1007/s00359-004-0518-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-004-0518-3

Keywords

Navigation