Warm Microgradients Elicit Adaptive Behavior in Isotropically Cooled, Inert Populations of Oxytricha bifaria (Ciliophora, Hypotrichida)
Corresponding Author
FILIPPO BARBANERA
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Corresponding Author: F Barbanera-Telephone number: 0039-50-500840; FAX number: 0039-50-24653; Email: [email protected]Search for more papers by this authorFABRIZIO ERRA
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Search for more papers by this authorNICOLA RICCI
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Search for more papers by this authorCorresponding Author
FILIPPO BARBANERA
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Corresponding Author: F Barbanera-Telephone number: 0039-50-500840; FAX number: 0039-50-24653; Email: [email protected]Search for more papers by this authorFABRIZIO ERRA
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Search for more papers by this authorNICOLA RICCI
Dipartimento di Etologia, Ecologia ed Evoluzione, via A. Volta, 6-56126 Pisa, Italy
Search for more papers by this authorABSTRACT
In order to investigate the physiological potentialities of behaviorally inert Oxytricha bifaria, cooled from 24 to 9° C according to an already standardized protocol, a warm microgradient was created in the experimental chamber and the behavior of ciliates was analyzed both at the level of the passing warm wave front (dynamic microgradient), and, afterwards, when the thermal gradient stabilized (static microgradient). We monitored the general behavior of the experimental populations by means of (i) their centroid, (ii) the ethograms of single oxytrichas, and (iii) calculating the numerical indices and rates of their creeping tracks. It was found that (a) the population moves towards the heating source, (b) the oxytrichas react immediately to the thermal stimulus, (c) creeping forwards (d) at very high velocity (e) along uninterrupted looping tracks (f) according to precise mechanisms of positive/negative orthokinesis, thus orientating towards the environmental optimum. Moreover, (g) the ciliates accumulate in the warmest area, correcting their creeping by means of many specific behavioral patterns (the Side Stepping Reaction) once the gradient is stabilized. At 9° C, despite their inertness, the ciliates are still able to behave adaptively reacting immediately and orientatedly, once a directional factor (the thermal gradient) arises in an isotropic environment.
References
-
Banks, C. J.
1957. The behaviour of individual coccinellid larvae on plants.
Br. J. Anim. Behav., 5: 12–24.
10.1016/S0950-5601(57)80039-2 Google Scholar
-
Bell, W. J.
1990. Searching behaviour. The behavioural ecology of finding resources. Chapman & Hall,
London
. p.
83–94.
10.1007/978-94-011-3098-1_7 Google Scholar
- Carlson, F. D. 1962. A theory of the survival value of motility. In: D. W. Bishop, (ed.), Spermatozoan Motility. Am. Assoc. Adv. Sci., Washington , D. C. p. 137–146.
- Connolly, J. G., Brown, I. D., Lee, A. G. & Kerkut, G. A. 1985. The effects of temperature upon the electrophysiological properties of Tetrahymena pyriformis-NT1. Comp. Biochem. Physiol., 81A: 293–302.
- Diehn, B., Feinlieb, M., Haupt, W., Hildebrand, E., Lech, E & Nultsch, W. 1977. Terminology of behavioral responses of motile microorganisms. Photchem. Photobiol., 26: 559–560.
- Eibl-Eibesfeldt, I. 1967. Grundriss der Vergleichenden Verhaltensforschung Ethologie. R. Piper, Verlag, München p. 1–529.
- Fenchel, T. 1987. Ecology of Protozoa. The Biology of Free-Living Phagotrophic Protists. Science Tech Publishers, Madison , Wisconsin . p. 1–193.
- Glaser, O. 1924. Temperature and forward movement of Paramecium. J. Gen. Physiol., 7: 177–188.
- Hennessey, T. & Nelson, D. L. 1979. Thermosensory Behaviour in Paramecium tetraurelia: a Quantitative Assay and Some Factors that Influence Thermal Avoidance. J. Gen. Microbiol, 112: 337–347.
- Hennessey, T., Saimi, Y. & Kung, C. 1983. A heat induced depolarization of Paramecium and its relationship to thermal avoidance behaviour. J. comp. Physiol., 153: 39–46.
- Hildebrand, E. 1978. Ciliary Reversal in Paramecium: Temperature Dependence of K+-Induced Excitability Decrease and of Recovery. J. comp. Physiol, 127: 39–44.
- Inoue, T. & Nakaoka, Y. 1990. Cold-Sensitive responses in the Paramecium Membrane. Cell Struct. Funct., 15: 107–112.
-
Jahn, T. L. &
Bovee, E. C.
1967. Motile Behavior of Protozoa. In: T T. Chen, (ed.), Research In Protozoology. Pergamon Press,
Oxford
,
London
. 1: 41–200.
10.1016/B978-0-08-011846-8.50005-0 Google Scholar
- Jennings, H. S. 1904. Reactions to heat and cold in the ciliate infusoria. Contribution to the study of the behaviour of lower organisms. Carnegie Institute of Washington, Publications, 16: 5–28.
- Jennings, H. S. 1906. Behaviour of the Lower Organisms. Indiana University Press, Bloomington , London , p. 1–366.
- Kittredge, J. S. 1980. Behavioral bioassays: the range of response thresholds. In: A. D. McIntyre & J. B. Pearce, (ed.), Biological Effects of Marine Pollution and the Problems of Monitoring. Proc. Ices Workshop held in Beaufort, North Carolina, Conseil International pour 1′ Exploration de la Mer, Copenhague , Danemark . p. 152–153.
- Machemer, H. 1972. Temperature influences on ciliary beat and meta-chronal coordination in Paramecium. J. Mechanochem. Cell Motility, 1: 57–66.
- Machemer, H. 1974. Frequency and Directional Responses of Cilia to Membrane Potential Changes in Paramecium. J. comp. Phyiol, 92: 293–316.
- Machemer, H. 1989. Cellular Behaviour Modulated by Ions: Electrophysiological Implications. J. Protozool., 36: 463–487.
- Machemer, H. 1996. Behavior of protozoa. In: K. Hausmann & N. Hüllsmann, (ed.), Protozoology, 2nd ed. Georg Thieme Verlag, Stuttgart , New York . p. 260–271.
- Machemer, H. & Teunis, P. F. M. 1996. Sensory-Motor Coupling and Motor Responses. In: K. Hausmann & P. C. Bradbury, (ed.), Ciliates: Cells as Organisms. Gustav Fischer, Stuttgart , p. 379–402.
- Martinac, B. & Machemer, H. 1984. Effects of varied culturing and experimental temperature on electrical membrane properties in Paramecium. J. exp. Biol., 108: 179–194.
- Matsuoka, T., Mamiya, R. & Taneda, K. 1990. Temperature-Sensitive Responses in Blepharisma. J. Protozool., 37: 323–328.
- McFarland, D. J. 1990. What It Means for Robot Behaviour to be Adaptive. In: J. A. Meyer & S. W. Wilson, (ed.), From Animals to Animats, Massachusetts Institute of Technology Press, Cambridge , Massachusetts , London England . p. 22–28.
-
Mendelssohn, M.
1895. Über den Thermotropismus einzelliger Organismen.
Pflüger's Arch. Ges. Physiol., 60: 1–27.
10.1007/BF01661667 Google Scholar
- Mendelssohn, M. 1902a. Recherches sur la thermotaxie des organismes unicellulaires. Journal de Physiol, et de Pathol. Génér., 4: 393–409.
- Mendelssohn, M. 1902b. Recherches sur l'interférence de la thermotaxie avec d'autres tactismes et sur le mécanisme du mouvement thermotactique. Journal de Physiol, et de Pathol. Génér., 4: 475–488.
- Mendelssohn, M. 1902c. Quelques considérations sur la nature et le rôle biologique de la thermotaxie. Journal de Physiol, et de Pathol. Génér., 4: 489–496.
- Meyer, J. A. & Guillot, A. 1990. From animals to animats: everything you wanted to know about the simulation of adaptive behavior. Tech. Rep. BioInfo (Ecole Normale Supérieure, Paris, France), 1: 1–40.
- Nakaoka, Y. & Oosawa, E 1977. Temperature-Sensitive Behavior of Paramecium caudatum. J. Protozool, 24: 575–580.
- Nakaoka, Y., Kurotani T. & Itoh, H. 1987. Ionic mechanism of ther-moreception in Paramecium. J. exp. Biol, 127: 95–103.
- Ricci, N. 1981. The ethogram of Oxytricha bifaria (Ciliata, Hypotrichida). The motile behaviour. Acta Protozool, 20: 393–410.
- Ricci, N. 1990. The behaviour of ciliated protozoa. Anim. Behav., 40: 1048–1069.
- Ricci, N. 1996. Ethology of Ciliates. In: K. Hausmann & P. C. Bradbury, (ed.), Ciliates: Cells as Organisms. Gustav Fischer, Stuttgart , p. 403–416.
- Ricci, N. & Erra, F. 1995. The Crowding Effect: an ethologic Analysis. Eur. J. Protistol., 31: 302–308.
- Ricci, N., Banchetti, R. & Cetera, R. 1980. Messa a punto di una tecnica di cultura per il ciliato ipotrico Oxytricha bifaria Stokes. Atti Soc. Tosc. Sci. Nat. Mem., 87: 211–218.
- Ricci, N., Barbanera, F. & Erra, F. 1998a. The Effects of Cooling Conditions on the Behavior of Oxytricha bifaria (Ciliata, Hypotrichida). J. Eukaryot. Microbiol, 45: 381–391.
- Ricci, N., Barbanera F. & Erra, E 1998b. A Quantitative Approach to Movement, Displacement and Mobility of Protozoa. J. Eukaryot. Microbiol., 45: 606–611.
- Ricci, N., Erra, E., Russo, A. & Banchetti, R. 1989. Substrates determine spatial distribution of Oxytricha bifaria (Ciliata, Hypotrichida). J. Protozool., 36: 567–571.
- Sollberger, A. 1962. General properties of biological rhythms. Ann. N. Y. Acad. Sci., 98: 757–774.
- Stock, C., Krüppel, T. & Lueken, W. 1997. Kinesis in Euplotes vannus-Ethological and Electrophysiological Characteristics of Chemosen-sory Behavior. J. Eukaryot. Microbiol., 44: 427–433.
- Tawada, K. & Miyamoto, H. 1973. Sensitivity of Paramecium Thermotaxis to Temperature Change. J. Protozool., 20: 289–292.
- Tawada, K. & Oosawa, F. 1972. Responses of Paramecium to Temperature Change. J. Protozool, 19: 53–57.
- Tominaga, T. & Naitoh, Y. 1992. Membrane potential responses to thermal stimulation and the control of thermoaccumulation in Paramecium caudatum. J. exp. Biol., 164: 39–53.
- Van Houten, J. 1979a. Chemosensory behavior in protozoa. In: M. Lev-andowsky & S. H. Hunter, (ed.), Biochemistry and Physiology of Protozoa. 2nd ed. Academic Press, New York . 4: 67–124.
- Van Houten, J. 1979b. Membrane Potential Changes During Chemo-kinesis in Paramecium. Science, 204: 1100–1103.
