Escape Response of Euplotes octocarinatus to Turbellarian Predators

Arch. Protistenkd. 144 (1994): 163-171 © by Gustav Fischer Verlag Jena

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Escape Response of Euplotes octocarinatus to Turbellarian Predators HANS-WERNER KUHLMANN Institute for General Zoology and Genetics, University of Munster, Germany Summary: Physical contact between the freshwater ciliate Euplotes octocarinatus and its turbellarian predator, Stenostomum sphagnetorum, elicits a behavioural response of the potential prey which is different from the normal "avoiding reaction" of Euplotes. Because of its defensive character it is called "escape response". The response was analysed by the use of a video camera and recorder system. It was found that the escape response takes a regular course, beginning with sudden backward moving of Euplotes, followed by a rapid turn around and a subsequent forward movement. Velocities during the escape response are 1 to 5 times higher than calculated for control cells. The whole reaction lasts about 2 s. Within this time a Euplotes cell moves more than 1,000 IJm away from its predator. While 90 % of well-fed Euplotes cells demonstrated the defensive response, starved cells cultivated separately from their predators revealed fewer escape responses, however, several of the starved cells regained the capacity for the escape response after exposure to Stenostomum or Stenostomum-conditioned medium for 20 h. It is discussed whether or not the inducible behavioural response is triggered by the same predator-released substances that are known to induce defensive morphological changes in Euplotes. Key Words: Anti-predator tactics; Behavioural response; Predator-induced defense; Euplotes octocarinatus; Stenostomum sphagnetorum.

Introduction The relationship between a predator and its prey is of fundamental ecological interest. Through the analysis of numerous individual encounters some general strategies employed in defense have become understood. Well known examples are the evolution of mimicry or the principles of coloration (HUMPHRIES & DRIVER 1970). Comparatively little, however, is known about tactics of prey species that reduce their mortality from predation by timing their activities to avoid their predators, by developing predator-resistant morphologies or chemical defenses in response to cues emitted by their predators, or by evolving special escape behaviours. Predator-induced defenses in aquatic communities have been reported for barnacles, bryozoa, cladocera, rotifers

and protozoa (HAVEL 1987 for review). In all these cases the prey is sensitive to stimuli from predators which cause a change in the prey's morphology that protects it against predation. Among protozoa, predator-induced morphological changes have been described for several species of the hypotrich ciliate Euplotes (KUHLMANN & HECKMANN 1985), for the hypotrich Onychodromus quadricornutus (WrcKLow 1988), and for the tetrahymenid ciliate Lambornella clarki (WASHBURN et al. 1988). Cells of Euplotes octocarinatus, within a few hours of exposure either to predatory protozoa or to turbellarians as Stenostomum sphagnetorum, develop prominent lateral "wings" and protuberant dorsal and ventral ridges. The changes in

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cell architecture are mediated by a reorganization of the microtubular cytoskeleton (JERKA-DzIADOSZ et al. 1987) and are perpetuated as long as the concentration of the morphogen is maintained. The extent of transformation depends on the concentration of signal molecules (KUSCH 1993b). In addition to the morphological response, cells of Euplotes show a defensive behavioural response that is initiated by direct contacts with Stenostomum (KUHLMANN 1991). It was the intention of this study to analyse this striking behavioural reaction of Euplotes. As it is different from the typical "avoiding reaction" in its intensity and its course and as it occurs only after physical contact with Stenostomum, it is called "escape response" (see also the Discussion). A comparable predator-induced behavioural response has been mentioned for only one other protozoan species (WICKLOW 1988); The behavioural response of Euplotes becomes even more interesting with the finding, that it is inducible in starved cells by a predator-released factor and, therefore, seems to be a previously unknown variation of predator-induced defense.

were analysed. Locations of the cells were marked frame by frame on the video screen and the paths were traced. The following information was calculated (see Figs. 1-3): I) the speed of a forward moving Euplotes cell (from a to b) before contacting Stenostomum; 2) the angle a. by which a forward moving Euplotes cell contacted Stenostomum; 3) the distance (b-c) Euplotes travelled backward until it turned around and changed to forward movement again; 4) the angle 13 by which a backward moving Euplotes cell left Stenostomum; 5) the speed of a backward moving Euplotes cell during the first part of the escape response (from b to c); 6) the distance (c-d, see Results for definition) Euplotes travelled during the second part of the escape reaction; 7) the angle y of a forward moving Euplotes cell during the

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Cells of lines 1(6)-VI, 69(2)-VII and 68(2)-VIII of Euplotes octocarinatus were employed in this study. For origin of strains and method of cultivation see KUHLMANN & HECKMANN (1989). Stenostomum sphagnetorum was isolated from a freshwater pond close to the town of MUnster, Germany, and kept at 20°C in glass vessels partially filled with the synthetic salt medium, SMC (KUHLMANN & HECKMANN 1989). Animals were fed three times per week with the ciliate Colpidium campylum cultivated in a wheat straw infusion at 26°C and washed free of the infusion before feeding.

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Video-recording of the escape response Escape responses of Euplotes from Stenostomum were analysed using the Sony color video camera DXC-lOIP, the Sony videocassette recorder VO-5630 which records 625line/50-field monochrome video signals and the Sony Trinitron colour video monitor PVM-137IQM. The camera was installed on a Zeiss photomicroscope. Escape responses were documented using phase contrast optics at low magnification. The temperature was adjusted at 20°C.

Videofilm analysis By playback of the videofilm still pictures of contacts between Euplotes and Stenostomum and escape responses

Figs. 1-3. Schematic representation of an escape response of Euplotes triggered by contact with Stenostomum (Fig. 1) and the parameters that have been determined or calculated (Figs. 2, 3). Fig. 1: The different positions of Euplotes before, during and after the escape response are designed as a, b, c, and d. Euplotes moves forward at first from a to b; then - at the beginning of the escape response in b - it rapidly moves backward until it reaches c where the cell turns around and finally moves forward again to position d (for definition see Results). Angular degrees that have been determined are given in Fig. 2, distances travelled by Euplotes that have been measured and used to calculate mean velocities as well as the straigth-line distance between start and finish of the whole response (smaller line between b and d) are presented in Fig. 3.

Escape Response of Euplotes

second part of the escape response; 8) the speed of Euplotes during the second part of the escape response (from c to d); 9) the straight-line distance between the start and the finish of the whole response (b-d); and 10) the duration of the whole response. In all these calculations, movements of Euplotes were assumed to occur in only two dimensions. The assumption is generally reasonable because Euplotes and its predators were maintained in a shallow container and remained in focus throughout each response. However, in exceptional cases at the end of an escape response movements in the third dimension occurred, causing underestimates of distances travelled and angular changes in direction (see GILBERT 1985).

Results Documentation and analysis of the escape response For video recording and analysing major features of the escape response of Euplotes such cells of E. octocarina-

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tus were chosen that had been cultivated together with Stenostomum for at least 24 h. These cells had been transformed into the "circular form" with extended lateral wings under the influence of a predator released factor (see KUSCH 1993 a). Euplotes as well as Stenostomum were well-fed and moved forward on a slide at relatively constant velocities during video recording. Under these experimental conditions escape responses of Euplotes appeared regularly if a Euplotes cell contacted Stenostomum with its anterior cell pole, but they appeared only exceptionally if Euplotes contacted Stenostomum with one of its sides or with its posterior pole (Fig. 4). The escape response of Euplotes can be characterized as: 1) a rapid backward moving, 2) a tum around, and 3) a subsequent forward movement still at a relatively high velocity (see also Materials and Methods). Under normal culture conditions - without any predator - cells of E. octocarinatus never showed such a behaviour, but instead a weak "avoiding reaction": When a Euplotes cell meets another one or moves against something impassa-

Fig. 4. S. sphagnetorum together with its prey E. octocarinatus (in its circular form). Moving direction of Euplotes is indicated by the arrow. An escape response will be expected only if Euplotes touches Stenostomum with its anterior cell side. The mouths (m) of Stenostomum are clearly visible (S. sphagnetorum typically glides on the substrate on its dorsal side).

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Figs. 5-19. Three sequences - each of five consecutive frames of a videofilm (Figs. 5-9, Figs. 10-14, Figs. 15-19) - documenting five escape responses of E. octocarinatus after contact with S. sphagnetorum. Escaping cells (no. 1-5) are marked by solid or open triangles, control cells (no. 6-8) that had no contact with Stenostomum are marked by arrows. Fig 5. Cell no. I moves backward. Fig. 6. The cell turns around. Figs. 7-9. Euplotes rapidly moves forward again. Fig. 10. Two cells (no. 2 and 3) just before contacting Stenostomum. Fig. 11. The same cells soon after contact rapidly moving backward. Fig. 12. Both cells synchronously turn around. Figs. 13-14. The cells at forward moving. Fig. 15. Cells no. 4 and 5 before contact with their predator. Fig. 16. Cell no. 4 moves backward after contact to Stenostomum, cell no. 5 at the moment of contact. Fig. 17. Both cells just begin to turn around. Figs. 18-19. The cells move forward again into opposite directions.

ble, the cell usually changes its creeping direction without rapid backward movement and a subsequent turn around; in the few cases a cell moves backward this happens at normal velocities and always over short distances (50-250 /lm). Non-transformed ovoid shaped Euplotes cells, as well as transformed ones in their circular form, show an escape response only if they have physical contact with S. sphagnetorum (or with several other species of turbellarians), but do not show such a behaviour spontaneously, or if they contact other Euplotes cells or, e.g., annelids (Aeolosoma variegatum, which is of similar size as S. sphagnetorum, was tested). In Figs. 5-19 escape responses of five cells of E. octocarinatus after contact with Stenostomum are documen-

ted. The directions and distances the cells travelled during the escape responses are shown in Fig. 20. They are compared with the traces of three cells that had no contact to a predator. It can be seen that the escaping cells as well as the control cells move on curves pointing to the right, the escaping cells covering at the same time considerably longer distances. In Table 1 major features of the escape response of Euplotes are summarized. For this information only physical contacts of Euplotes at Stenostomum's left side have been analysed (because only for left-side contacts the angles a-y have been defined in Fig. 2). Contacts near the mouth region of Stenostomum have also been disregarded as captured Euplotes, which were too large to be ingested, often were pushed away by Stenostomum.

Escape Response of Euplotes

Fig. 20. Cell movements of escaping E. octocarinatus after contact to Stenostomum (no. 1-5, see Figs. 5-19) and at normal travelling (no. 6-8, see Figs. 5-19). The start is indicated by an asterisk in each case. Continuous broken lines show backward moving, solid lines trace forward moving.

Table 1. Major features of the escape response of E. octocarinatus cells that contacted S. sphagnetorum (see also Figs. 1-3). Mean') Velocity before contact (/lm x S-I) Angle a (angular degrees) Distance travelled backward (/lm) Angle ~ (angular degrees) Velocity during backward movement (/lm x S-I) Distance travelled forward (/lm) Angle 'Y (angular degrees) Velocity during forward movement (/lm x S-I) Straight line distance (/lm) (see Fig. 2) Duration of the whole response (s)

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movements that appeared in the third dimension (visible by the fact that the cell was no longer in focus), or by the criterion that an escaping cell reached a position at which the angle 'Y became "0" (see Fig. 2). The average creeping speed of a Euplotes cell (on the bottom of the glass vessel) is about 250 /lm x S-I before a contact with Stenostomum, while it is nearly five times higher during backward moving after a contact and still nearly double compared to normal creeping speed during the subsequent forward moving (Table 1). The distance of backward moving is about 500 /lm, whereas the distance of forward creeping during the second part of the escape reaction is more variable and extends from about 500 /lm to about 1,000 /lm. The angle a by which a Euplotes cell approaches Stenostomum is similar to the angle ~ by which Euplotes flees from its predator before the cell orients to the right. However, if the angle a tends to be rather acute so that Euplotes touches its predator with its side instead of its anterior pole, in some cases no escape response will be initiated. The same holds true for Euplotes cells that have contact with Stenostomum at their posterior pole, as is shown in Figs. 21-24. In such cases Euplotes may increase its speed a little with retention of its direction, however, such a behaviour is quite different from the escape response defined above.

Correlation between escape response and feeding condition of Euplotes Under good feeding conditions more than 95 % of Euplotes cells that had been cultivated together with Stenostomum for at least 24 h showed escape responses when contacting Stenostomum. Well-fed Euplotes cells that never had any prior contact with Stenostomum or Stenostomum-conditioned medium were able to initiate escape responses in almost 90 % of cases. While the cells of the first group - which expressed their circular form and therefore could hardly be swallowed by their

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While the distance of backward movement of an escaping Euplotes cell (from b to c in Fig. 3) could easily be measured, the distance of the subsequent forward moving (from c to d in Fig. 3) was difficult to determine in several cases, because the position "d" is not fixed by a clear behavioural change of Euplotes. Therefore, the end of an escape response was defined by the occurrence of one out of the following three criteria: The position "d" is reached either by the first halt of an escaping cell (usually the duration of such a halt was 0.2-0.5 s), by

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Figs. 21-24. Sequence of four consecutive frames of a videofilm documenting a contact of E. octocarinatus with S. sphagnetorum that did not initate an escape response in the prey. Fig. 21. Euplotes (triangle) before contact with Stenostomum. Fig. 22 Euplotes having contact wiht the turbellarian with its right posterior cell side. Figs. 23-24. Euplotes still moves forward without showing the response.

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predators - continued to show the escape response over a period of 7 days without feeding, the cells of the second group - which had been cultivated separately and therefore expressed their nonnal ovoid shape - progressively lost this ability when they were starved. 80 % of Euplotes cells of the first group still showed the response on the 7th day without food, whereas fewer than 40 % of cells of the second group responded at the 7th day of starvation (Fig. 25). Therefore, it is concluded that the feeding condition of non-transfonned Euplotes cells is of importance with regard to their capacity to undergo an escape response, in contrast to transfonned cells, which maintain their capability to flee from their predators if they become starved.

Does the escape response of Euplotes contribute to the predator-induced morphological defense? To find out whether Stenostomum induces its starved prey Euplotes to undergo escape responses, cells of E. octocarinatus were cultivated separately from its predator without allowing them to feed during 7 days. After that time Euplotes was mixed with Stenostomum and the percentages of initiated escape responses were measu-

red. Fig. 26 shows that directly after mixing turbellarians and ciliates about 40 % of the Euplotes cells showed escape responses. Generally, the escape response was weaker than that of well-fed cells. During the next 20 hours of co-culturing in the absence of any food the escape response became stronger in most of the cells that were able to initiate it. The percentage of escape responses initiated in Euplotes increased from 45 % to 75 %. This increase was not caused by selection, as was ensured by calculating cell densities of Euplotes before and after the experiment (Stenostomum was fed with a surplus of Colpidium before and during the experiment, so that the turbellarians did not feed on Euplotes). Therefore, it is concluded that the escape response of E. octocarinatus can be induced in those cells that already have lost their escape response capacities after a period of starvation by co-culturing the Euplotes with its predator. A similar experiment was perfonned using conditioned medium instead of living turbellarians as a means of inducing the capacity to show an escape response. Starved cells of E. octocarinatus were exposed to the conditioned medium and tested every four hours for their capacity to undergo escape responses in direct contacts to their predator. The result was a lower increase of the percentage of initiated escape responses in Euplotes, this time from less than 40 % to almost 70 % (Fig. 26).

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Escape Response of Euplotes

Discussion The purpose of the present study was to describe and analyse a defensive response of E. octocarinatus to predatory turbellarians and to find out whether or not the reaction is a kind of inducible defense. PHILLIPS (1977) has differentiated defensive responses into "avoidance responses", which are behavioural responses resulting from the detection of distant enemies, and "escape responses", which are behavioural responses resulting from physical contact with enemies. As the defensive response of Euplotes is initiated exclusively by direct mechanical contact to Stenostomum, it is termed "escape response". In contrast to the definition of PHILLIPS a well known behavioural reaction of Paramecium, which is similar to the escape response of Euplotes, but is not initiated by predators, has been termed "avoiding reaction" by JENNINGS (1906): A Paramecium cell, in responsive to a mechanical disturbance, swims rapidly backwards. Backward swimming declines in speed and eventually comes to a halt, while Paramecium spins about its longer axis. The cell gradually resumes forward locomotion during circling and finally normalizes its behaviour showing the typical forward swimming helix (MACHEMER & SUGINO 1989). Mechanical-pulse stimulation and recording of the electric membrane events showed that deformation of the anterior cell end elicits a depolarizing receptor potential which triggers a graded action potential (NAITOH & ECKERT 1969). A raised K concentration (or other depolarizing condition) also induces backward swimming in Paramecium. A positive shift of the K equilibrium potential following raised [Kl o depolarizes the membrane potential which successively induces backward swimming (MACHEMER & SUGINO 1989). Touching Paramecium at the posterior cell end leads to an acceleration of forward swimming (JENNINGS 1906) and a slightly different kind of escape response. "Avoidance reactions" have also been reported for other protozoa (APPLEWHITE 1979, for review). Well known are experiments performed with Stylonychia mytilus which revealed an "avoidance" of rough surfaces, as only 10--40 % of cells occurred on a rough "chessboard" compared with a smooth one of the same size. Well-fed cells showed a more pronounced and longer lasting avoidance (MACHEMER & DEITMER 1987). In this respect the reaction of Stylonychia is comparable to that one of Euplotes analysed in this study. Behavioural responses of protozoa to surface-bound cues have been reported several times (see VAN HOUTEN et al. 1981). Most of them, however, deal with food or mate recognition. To my knowledge, only one account exists mentioning a behavioural response of a protozoan to its predator (WICKLOW 1988): The hypotrich ciliate Onychodromus quadricornutus is stimulated by sub-

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stances released by cannibal giants of the same species for defensive spine growth. When cannibal giants have physical contact with a potential prey cell, "there is an immediate avoidance reaction by the prey cell and an attack response by the predator in the form of increased forward speed". WICKLOW (1988) gives no further information concerning distances travelled by the escaping prey or concerning its velocities. Following the definition of PHILLIPS (1977), the reaction of Onychodromus is - as that one of Euplotes - an "escape response" instead of an "avoidance reaction". It is remarkable that it occurs in a species that - as Euplotes - is capable to express a different morphotype under the influence of its predators (giants of Onychodromus and cells of Lembadion magnum). Among rotifers, escape responses seem to be rather common. Planctonic rotifer species belonging to the genus Polyarthra posses appendages - called paddles that permit the small, soft-bodied rotifer to jump considerable distances very rapidly and escape from a variety of invertebrate predators which make contact with it. Direct laboratory observations have shown that the escape responses of Polyarthra are very effective against predatory rotifers of the genus Asplanchna (GILBERT 1980). The same seems to be true for the efficiency of the escape response of E. octocarinatus (KUHLMANN 1990). The escape response of Polyarthra was cinematographically analysed by GILBERT (1985). It can be characterized by a very short lag time, great velocity, considerable displacement and - in contrast to the escape response of E. octocarinatus - by its unpredictable directionality, which seems to be widespread among prey animals (HUMPHRIES & DRIVER 1979). Avoidance and escape responses of asteroid species and molluscs to predatory asteroids have also been studied for some time (PHILLIPS 1977; VAN VELTHUIZEN & OAKES 1981). As in rotatoria, in all these cases the behavioural responses occur obviously spontaneously and do not seem to be triggered by the predator. In well-fed cells of E. octocarinatus reared without predators, the escape responses appear spontaneously in the majority of cells, that have physical contact to Stenostomum. In starved cells, however, the situation is different, because only about 40 % of the cells are initiated for the response by first contacts to their predator. When, however, the latter cells - still under hunger conditions were exposed to their predator for a defined period, the percentage of cells initiated for an escape response increased to 70 %. Because of this fact the escape response of Euplotes to Stenostomum must be considered as a new variation of predator-induced defense. This behavioural change of Euplotes seems to go hand in hand with defensive morphological changes in the same species (see KUHLMANN & HECKMANN 1985). Both, the physiological as well as the morphological transforma-

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tion of Euplotes are induced not only by the predator itself, but also - to lesser extend - by predator-conditioned medium. The time of exposure of Euplotes to Stenostomum or to its conditioned medium that is necessary to establish either the morphological or the physiological transfonnation is almost the same (4-20 h, dependent on the degree oftransfonnation; see also KUSCH 1993b). Moreover, morphological transformation as well as a behavioural change in Euplotes are induced by the same turbellarian or protozoan predators. Recently, KUSCH found out (personal communication) that Amoeba proteus (another predator of Euplotes) is capable to induce very similar morphological and behavioural transformations in cells of E. octocarinatus. The morphological as well as the behavioural changes occurred within about 20 h in those cells that either had physical contact to the amoebae or to A. proteus-conditioned medium. Transformed cells of E. octocarinatus were less frequently eaten by the amoebae than non-transformed ones. It could be demonstrated that it is the behavioural response, and not the morphological transfonnation, that protected co-cultured cells of E. octocarinatus from A. proteus (KUSCH, personal communication). It is still unknown whether the factors causing the behavioural defensive response in Euplotes are identical with the factors responsible for the morphological defense, which recently have been shown to be polypeptides (KUSCH & HECKMANN 1992; KUSCH 1993a). Nothing is known at present about the mechanisms which are responsible for the predator-induced enhancement of the capacity to undergo escape reactions in Euplotes. Perhaps specific mechanoreceptors - situated at the cell surface of Euplotes - are involved in the recognition of a turbellarian predator and playa role in the initiation of the escape response of the prey. Such receptors should then be localized preferably at the anterior cell sides of Euplotes, e.g. at the cilia of the adoral band of membranelles, because the response of Euplotes is initiated especially in those cells that contacted Stenostomum with their anterior sides. It is also conceivable that Euplotes cells in their typical ovoid form have a reduced number of receptors compared with circular shaped transfonned cells, and that well-fed cells generally express a greater number of receptors compared to starved ones. By this assumption it could be explained, why ovoid, starved cells are less often induced to show an escape response compared to circular, well-fed cells. Presently, however, this is speculation. Recently, a few other defensive strategies of ciliates against their predators have been reported (MIYAKE et al. 1990; HARUMOTO & MIYAKE 1991). Nevertheless, preypredator interactions in protozoa are still poorly understood. Further studies are necessary which will provide new research opportunities for the biology of cell-cell interactions.

Acknowledgements: The author would like to thank Dr. J. KUSCH for valuable discussion and Drs. H.-D. GbRTZ, K. HECKMANN and T. KRuPPEL for their comments on the manuscript.

References ApPLEWHITE, P. B. (1979): Learning in protozoa. In: LEVANDOWSKY, M. & HUTNER, S. H. (eds.), Biochemistry and physiology of protozoa 4, 2nd ed., pp. 341-355. New York. GILBERT, J. J. (1980): Feeding in the rotifer Asplanchna: behavior, cannibalism, selectivity, prey defenses, and impact on rotifer communities. In: KERFOOT, W. C (ed.), Evolution and ecology of zooplankton communities, pp. 158-172. New England. - (1985): Escape response of the rotifer Polyarthra: a highspeed cinematographic analysis. Oecologia 66: 322-331. HARUMOTO, T. & MIYAKE, A. (1991): Defensive function of trichocysts in Paramecium. J. Exp. Zool. 260: 84-92. HAVEL, J. E. (1987): Predator-induced defenses: a review. In: KERFOOT, W. C & Sm, A. (eds.), Predation: direct and indirect impacts on aquatic communities, pp. 263-278. New England. HUMPHRIES, D. A. & DRIVER, P. M. (1970): Protean defence by prey animals. Oecologia 5: 285-302. JENNINGS, H. S. (1906): Behavior of the lower organisms. New York. JERKA-DzIADOSZ, M., DOSCHE, C, KUHLMANN, H.-W. & HECKMANN, K. (1987): Signal-induced reorganization of the microtubular cytoskeleton in the ciliated protozoon Euplotes octocarinatus. J. Cell Sci. 87: 555-564. KUHLMANN, H.-W. (1990): Zur Effizienz defensiver Zellveranderungen bei Euplotes. Verh. Deutsch. Zool. Ges. 83: 589-590. - (1991): Escape reactions of Euplotes induced by predatory turbellaria. J. Protozool. 38: 16A. - & HECKMANN, K. (1985): Interspecific morphogens regulating prey-predator relationships in protozoa. Science 227: 1347-1349. - (1989): Adolescence in Euplotes octocarinatus. J. Exp. Zool. 251: 316-328. KUSCH, J. (1993a): Predator-induced morphological changes in Euplotes (Ciliata): Isolation of the inducing substance releases from Stenostomum sphagnetorum (Turbellaria). ibid. 265: 613-618. - (1993b): Induction of defensive morphological changes in ciliates. Oecologia 94: 571-575. - & HECKMANN, K. (1992): Isolation of the Lembadionfactor, a morphogenetically active signal, that induces Euplotes cells to change from their ovoid form into a larger lateral winged morpho Developm. Genetics 13: 241-246. MACHEMER, H. & DEITMER, J. W. (1987): From structure to behaviour: Stylonychia as a model system for cellular physiology. In: CORLISS, J. O. & PATTERSON, D. J. (eds.), Progress in protistology 2, pp. 213-330. Bristol. - & SUGINO, K. (1989): Electrophysiological control of ciliary beating: a basis of motile behaviour in ciliated protozoa. Compo Biochem. Physiol. 94A: 365-374.

Escape Response of Eup[otes

MIYAKE, A., HARUMOTO, T., SALVI, B. & RIVOLA, V. (1990): Defensive function of pigment granules in Blepharisma japonicum. Europ. J. Protistol. 25: 310-315. NAITOH, Y. & ECKERT, R. (1969): Ionic mechanisms controlling behavioral responses in Paramecium to mechanical stimulation. Science 164: 963-965. PHILLIPS, D. W. (1977): Avoidance and escape responses of the gastropod mollusc Olivella biplicata (SOWERBY) to predatory asteroids. 1. Exp. Mar. BioI. Ecol. 28: 77-86. VAN HOUTEN, J., HAUSER, D. C. R. & LEVANDOWSKY, M. (1981): Chemosensory behavior in protozoa. In: LEVANDOWSKY, M. & HUTNER, S. H. (eds.), Biochemistry and physiology of protozoa 4, 2nd ed, pp. 67-124. New York. VAN VELDHUIZEN, H. D. & OAKES, V. J. (1981): Behavioral responses of seven species of asteroids to the asteroid predator, Solaster dawsoni. Oecologia 48: 214-220.

Arch. Protistenkd. 144 (1994): 171-172 © by Gustav Fischer Verlag Jena

ForSSNER, W.: Colpodea (Ciliophora). In: Protozoenfauna Vol. 4/l.Ed.: D. MATTHES. 798 pages, 2900 figures, 38 tables. Gustav Fischer Verlag, Stuttgart - Jena - New York 1993. Price: DM 295.00. ISBN 3-437-30677-4 (Stuttgart), 1-56081-351-2 (New York). Six decades have passed since the publication of ALFRED KAHL'S great standard work on the systematics and determination of ciliates. The number of described species has increased so vastly in this period that even specialists often have trouble finding their bearings within the overall ciliate system. Furthermore, taxonomy and systematics have been subject to numerous corrections and amendments which have taken them beyond the bounds of KAHL's systematics. The taxonomically untrained scientist, who is nevertheless reliant on accurate identification of specimens for his work was - and largely still

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WASHBURN, J. 0., GROSS, M. E., MERCER, D. R. & ANDERSON, J. R. (1988): Predator-induced trophic shift of a free-living ciliate: Parasitism of mosquito larvae by their prey. Science 240: 1193-1195. WICKLOW, B. J. (1988): Developmental polymorphism induced by intraspecific predation in the ciliated protozoon Onychodromus quadricornutus. J. Protozool. 35: 137-141. Accepted: April 2, 1993 Author's address: Dr. H.-W. KUHLMANN, Institut ftir Allgemeine Zoologie und Genetik der UniversiUit Mtinster, Schlossplatz 5, D - 48149 Mtinster, Germany.

Buchbesprechung

is - faced with the almost impossible task of undertaking his determinations on the basis of KAHL'S work and the widely scattered literature published in the last 60 years. Volume 4/1, Colpodea (Ciliophora), following on Volumes 2 and 7/1 of the series "Protozoenfauna", begun in 1988, has found its competent author in the person of WILHELM FOISSNER. The volume of this 798 page work, which at first glance would seem to be rather generously dimensioned for this class of ciliates, proves to be no more than adequate. The author complied with the classification suggested by SMALL & LYNN (1981) and himself in 1985 to discuss a total of 170 species. Four families (Bursaridiidae, Jaroschiidae, Reticulowoodruffiidae, Tectohymenidae) and eight genera are newly established, 23 new species described, numerous reclassifications and synonymizations at family, genus and species level as well as copious nomenclatural corrections are undertaken. The colpodeans have