Skip to main content
SpringerLink
Log in

Oscillating haemolymph ‘circulation’ in the butterflyPapilio machaon L. revealed by contact thermography and photocell measurements

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

  1. 1.

    Pulsing and streaming of haemolymph in the heart, aorta and perineural sinus of unrestrained, unnarcotizedPapilio machaon L. (Lepidoptera, Papilionidae) were studied. The interrelationships between heart activity, abdominal movements and activity of thoracic pulsatile organs in haemolymph transport were examined and the indirect effects of these activities on tracheal ventilation of the thorax evaluated.

  2. 2.

    A thermistor technique was developed to record haemolymph movements by their convective and conductive cooling effects at the cuticular surface of insects. In addition, the direction of pulses and of haemolymph flow was determined from temperature measurements, utilizing the temperature gradient along the body axis of basking butterflies.

  3. 3.

    The direction of heart peristalsis changes periodically and is coordinated with abdominal length changes which were recorded using a photocell. Abdominal expansion is accompanied first by a pause and subsequently by reverse beating of the heart. Abdominal expansion may play a leading role in backward haemolymph transport and cause periodic ventral haemolymph backflow through the perineural sinus. Such backflow is most vigorous during heart pauses. The rhythmic undulatory movements of the ventral diaphragm give rise to only slight thermal convective effects.

  4. 4.

    The oscillation of haemolymph between thorax and abdomen is documented on the basis of changes in thermal conduction of the thorax. The significance of periodic haemolymph volume reduction in the thorax for tracheal ventilation is discussed with special regard to the role of heartbeat reversal.

  5. 5.

    During the forward heart pulse periods the abdomen performs volleylike ventilatory movements. These do not cause streaming of haemolymph in the thoracic haemocoel, which at this time is shut off from the abdominal haemocoel by a valve mechanism. This valve, situated in the anterior abdomen, was examined histologically and by scanning electron microscopy.

  6. 6.

    The activity of the lateral thoracic pulsatile organs is regularly interrupted by pauses which occur most frequently during the second half of the heart's forward pulse period. The function of the pulsatile organs is discussed in relation to changing thoracic haemolymph content.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

PNS :

perineural sinus

PO :

accessory thoracic pulsatile organ

C-method :

conduction-convection measurement

T-method :

temperature measurement

References

  • Bayer, R.: Untersuchungen am Kreislaufsystem der Wanderheuschrecke (Locusta migratoria migratorioides R. et F., Orthopteroidea) mit besonderer Berücksichtigung des Blutdruckes. Z. Vergl. Physiol.58, 76–135 (1968)

    Google Scholar 

  • Beckel, W.E.: The morphology, histology and physiology of the spiracular regulatory apparatus ofHyalophora cecropia (L.) (Lepidoptera). Proc. 10th Int. Congr. Entomol.2, 87–115 (1958)

    Google Scholar 

  • Brocher, F.: Les organes pulsatiles méso- et métatergaux des Lépidoptères. Archs. Zool. Exp. Gen.58, 149–171 (1919)

    Google Scholar 

  • Brocher, F.: Étude éxpérimentale sur le fonctionnement du vaisseau dorsal et sur la circulation du sang chez les insectes. III. LeSphinx convolvuli. Archs. Zool. Exp. Gen.60, 1–45 (1920)

    Google Scholar 

  • Brocher, F.: Le méchanisme de la respiration et celui de la circulation du sang chez les insectes. Archs. Zool. Exp. Gen.74, 25–32 (1931)

    Google Scholar 

  • Buddenbrock, W. von: Blut und Herz. In: Vergleichende Physiologie, Vol. VI, pp. 1–466. Basel, Stuttgart: Birkhäuser 1967

    Google Scholar 

  • Carus, C.G.: Nachträgliche Bemerkungen über den Blut-Umlauf in den Kerfen, insbesondere den Blut-Umlauf in vollkommenen betreffend. Isis21, 478–480 (1828)

    Google Scholar 

  • Freudenstein, K.: Das Herz und das Cirkulationssystem der Honigbeiene (Apis mellifica L.). Z. Wiss. Zool.132, 404–475 (1928)

    Google Scholar 

  • Gerould, J.H.: Periodic reversal of heart action in the silkworm moth and pupa. J. Morphol.48, 385–431 (1929)

    Google Scholar 

  • Gerould, J.H.: Structure and action of the heart ofBombyx mori and other insects. Acta Zool. (Stockholm)19, 297–352 (1938)

    Google Scholar 

  • Graber, V.: Die Insekten, Bd. 1. München: Oldenburg 1877

    Google Scholar 

  • Heinrich, B.: Heat exchange in relation to blood flow between thorax and abdomen in bumblebees. J. Exp. Biol.64, 561–585 (1976)

    Google Scholar 

  • Hanegan, J.L.: Control of heart rate inCecropia moths; response to thermal stimulation. J. Exp. Biol.59, 67–76 (1973)

    Google Scholar 

  • Hessel, J.H.: A preliminary comparative anatomical study of the mesothoracic aorta of the Lepidoptera. Ann. Entomol. Soc. Am.59, 1217–1227 (1966)

    Google Scholar 

  • Hessel, J.H.: The comparative morphology of the dorsal vessel and accessory structures of the Lepidoptera and its phylogenetic implications. Ann. Entomol. Soc. Am.62, 353–370 (1969)

    Google Scholar 

  • Jones, J.C.: The circulatory system of insects. Springfield, Illinois: Thomas 1977

    Google Scholar 

  • Krogh, A.: Studien über Tracheenrespiration. II. Über Gasdiffusion in den Tracheen. Pfluegers Arch. Gesamte Physiol. Menschen Tiere179, 95–120 (1920)

    Google Scholar 

  • Lagerspetz, K., Perttunen, V.: Effect of temperature on the periodic heart beat reversal and heart rate inCorethra plumicornis (Diptera). J. Insect. Physiol.8, 621–625 (1962)

    Google Scholar 

  • McCann, F.V.: Unique properties of the moth myocardium. Ann. N.Y. Acad. Sci.127, 84–99 (1965)

    Google Scholar 

  • McCann, F.V.: Physiology of insect hearts. Annu. Rev. Entomol.15, 173–200 (1970)

    Google Scholar 

  • Miller, P.L.: Respiration-aerial gas transport. In: The physiology of insecta, Vol. VI. Rockstein, M. (ed.), pp. 345–402. New York, San Francisco, London: Academic Press 1974

    Google Scholar 

  • Miller, T.A.: Electrophysiology of the insect heart. In: The physiology of insecta. Vol. V. Rockstein, M. (ed.), pp. 169–200. New York, San Francisco, London: Academic Press 1974

    Google Scholar 

  • Moreau, R., Lavenseau, L.: Rôle des organes pulsatiles thoraciques et du coeur pendant l'émergence et l'expansion des ailes des Lépidoptères. J. Insect Physiol.21, 1531–1534 (1975)

    Google Scholar 

  • Plateau, F.: Recherches expérimentales sur les mouvements respiratoires des insectes. Mem. Acad. R. Belg.65, 1–219 (1884)

    Google Scholar 

  • Queinnec, Y., Campan, M.: Influence of sexual maturation on cardiac activity and reactivity ofCalliphora vomitoria. I. Cardiac activity. J. Physiol. (Paris)70, 457–466 (1975)

    Google Scholar 

  • Richards, A.G.: The ventral diaphragm of insects. J. Morphol.113, 17–47 (1963)

    Google Scholar 

  • Richards, S.A.: Temperature regulation. London, Winchester: Wykeham Publications 1973

    Google Scholar 

  • Tenney, S.M.: Observations on the physiology of the lepidopteran heart with special reference to reversal of the beat. Physiol. Comp. Oecol.3, 286–306 (1954)

    Google Scholar 

  • Wasserthal, L.T.: Herzschlag-Umkehr bei Insekten und die Entwicklung der imaginalen Herzrhythmik. Verh. Dtsch. Zool. Ges.1974, 95–99 (1975a)

    Google Scholar 

  • Wasserthal, L.T.: The rôle of butterfly wings in regulation of body temperature. J. Insect Physiol.21, 1921–1930 (1975b)

    Google Scholar 

  • Wasserthal, L.T.: Heartbeat reversal and its coordination with accessory pulsatile organs and abdominal movements in Lepidoptera. Experientia32, 577–578 (1976)

    Google Scholar 

  • Wasserthal, L.T., Wasserthal, W.: Innervation of heart and alary muscles inSphinx ligustri L. (Lepidoptera). Cell Tissue Res.184, 467–486 (1977a)

    Google Scholar 

  • Wasserthal, L.T.: Ein zentrales Hämolymphdruckventil im Insektenkörper und seine Bedeutung für die Tracheenventilation. Verh. Dtsch. Zool. Ges.1977, 276 (1977b)

    Google Scholar 

  • Wasserthal, L.T.: Pendelnde Hämolymphversorgung und Tracheenventilation im Schmetterlingsflügel. Verh. Dtsch. Zool. Ges.1978, 268 (1978)

    Google Scholar 

  • Weber, H.: Grundriß der Insektenkunde. Stuttgart: Gustav Fischer Verlag 1966

    Google Scholar 

  • Wigglesworth, V.B.: The principles of insect physiology. 7th edn. London: Capman & Hall 1972

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lehrstuhl für Spezielle Zoologie der Ruhr-Universität Bochum, Postfach 1021 48, D-4630, Bochum 1, Germany

    Lutz Thilo Wasserthal

Authors
  1. Lutz Thilo Wasserthal
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wasserthal, L.T. Oscillating haemolymph ‘circulation’ in the butterflyPapilio machaon L. revealed by contact thermography and photocell measurements. J Comp Physiol B 139, 145–163 (1980). https://doi.org/10.1007/BF00691029

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00691029

Keywords

Search

Navigation