Recent Observations on Neck Extensions in Folliculinids (Protozoa) 1

Transcription

1 Recent Observations on Neck Extensions in Folliculinis (Protozoa) 1 DONALD C. M ATIHEWS DESPITE species variations, the process of folliculini lorica formation is funamentally similar (Penar, 19'19; Anrews, 1923; Faure-Fremiet, 1932; Dewey, 1939; an Das, 1947). In all a motile, nonfeeing stage becomes attache, secretes a sac an neck, an graually metamorphoses into a sessile feeing stage characterize by peristomal lobes. Although in certain well-establishe colonies restrictive attachment areas may moify sac length, breath, an height, moifications in neck length an number of spiral whorls seem not to be thus affecte (Matthews, 1963). Despite the fact that certain folliculinis with poorly evelope necks (Ascobius simplex an Folliculina boltoni) seem not aversely affecte, nevertheless it is commonly assume that wellevelope necks an neck extensions affor some survival value; i.e., 'the entrance of preators an etritus is lessene. Although this is an engaging conjecture, actually long necks an neck extensions affor little avantage. Rather, such folliculin is, responing to current isturbance, contract their peristomal lobes, whereas short-neck forms, not so affecte, continue to fee. Since our knowlege of folliculinis is too meager to warrant conclusions as to why extensions are mae, our attention for the present might best be focuse on the stage ( or stages) of the life-cycle responsible for their formation. The purpose of this paper is to place in question the limite alternatives of existing theories, an to rekinle interest in a question unsolve since As previously state, on completion of a lorica a nonfeeing swimmer usually metamorphoses into a feeing. sessile organism characterize by peristomal lobes. It is generally 1 Department of Zoology, University of Hawaii. Contribution No Hawaii Marine Laboratory, University of Hawai i, Honolulu 14, Hawaii. Manuscript receive May 31, assume that, in nature, this organism respon sible for the lorica remains for some time its occupant. However, once the terminal lip is complete, a isturbe organism may sever its boy-attachment point an, without eveloping peristomal lobes or actually living in its lorica, may vacate it an subsequently begin the process anew. Usually, however, on completion of the terminal lip the organism withraws into its sac an, following a rest perio, metamorphoses into a sessile feeing stage. Uner laboratory conitions, this stage may last from one to several ays. This perio is followe by one of two possible courses: either metamorphosis results in a motile stage which vacates the original lorica; or, following binary fission, a istal portion metamorphoses into a motile stage whereas a proximal portion metamorphoses into a sessile stage which, for some time, occupies the original lorica. Thus, subsequent neck extensions might be the result of (1) the stage that secrete the original lorica, (2) the stage remaining in the original lorica following binary fission, (3) the stage leaving the originallorica following binary fission, or (4) a "new" swimmer (or swimmers) entering another lorica. Although most investigators agree on the general process of lorica formation, few agree on the stage of the life cycle responsible for neck extensions. An, espite the above possibilities, the formation of neck extensions is toay explaine in the light of limite alternatives : either they are the result of the sessile stage which secrete the originallorica, or they are the result of a "new" swimmer which enters an empty lorica. In ' a personal communication E. A. Anrews (1952) states: No one has seen extensions actually in the process of making, but Hazi (l95l} gives some pages of argument that they are mae 229

2 230 by swimmers locating in empty tests, while I maintain it is less improbable to imagine the ault can artempta seconary imperfect neck or even a 'rhir while welling in the ol test. Following Anrew's suggestion, glass plates to which were attache M etafolli culina anreu/si, M. norgari, Parafolliculina uiolaceae, an Lagotia viriis were brought into the laboratory an the following neck-exten sion possibilities were stuie: e f /3 5 J.I FIG. 1. Metafolliculina anrews; as viewe from the right sie showing: a, peristomal lobes ; b, extene boy; c, neck without extensions;, nucleus; e, sac; an f, boy attachment point; PACIFIC SCIENCE, Vol. XVIII, April Neck Extensions ' by the Stage that secrete the Lorica. Although living M. anrewsi an M. norgari (Matt hews, 1963 ) with an without extensions were present, these were ignore for the moment because, even if subsequent neck extensions were forme, the possibility remaine that these coul be the prouct of some stage other than that which secrete the lorica; for example, a new swimmer ( or swimmers) that ha entere an empty lorica. To exclue ' this possibility the aquarium in which these plates were hel was completely covere with black paper except for one small area in which unetche glass slies were place. By this metho the entire lorica-forming process of M. anrewsi was observe. Thus it was mae certain that the folliculini occupying a particular lorica was inee its original builer. Metamorphosis of these original Iorica builers into swimmers was frequently observe an, as each swimmer vacate its lorica, a small, but easily istinguishable boy attachment point ( Fig. 5) was left in the proximal region of the empty sac. Likewise, binary fission an the subsequent metamorphoses into sessile an motile stages was observe. In such instances the original boy attachment point appeare unaltere either as to size, shape, position, or number. In approximately 25 M. anrewsi, only one instance of a neck extension was observe. This particular folliculini was brought to my attention by my inability to bring int o sharp focus the region just istal to the lip. When first observe at 8:25 AM the organism, with a single point attachment, lay contracte in the proximal en of its sac. Slowly it relaxe an extene its peristomal lobes above the cloulike, viscous mass which surroune the lip, only to contra ct again into the sac. The relaxation of the boy an the freeing of the perisrornal lobes above the istal opening of the neck ha been observe frequently in other specimens of M. anrewsi. In such instances, as the boy relaxe the spirally twiste peristornal lobes were carrie aloft where their pectinellae burst into a "running flame" of activity resembling the spiral ignition of a gas stove burner. In the present specimen such was not the case. As the boy relaxe ( Fig. 2g) an the peristomal lobes (a,

3 Neck Extensions in Folliculinis-MATTHEWS,----- a b c e f.' g 100 ~ FIG. 2. M eta/olliculina,anrewsi showing : a, slight, istal fol of right peristomal Iobe ; b, inistinct, istal region of neck extension; c, left peristomal lobe curve in a semicircle at right angles to main, longituinal axis of neck;, istinct, proximal region of neck extension; e, lip of neck; i. neck; an g, portion of boy. c) were carrie aloft, sometimes the right lobe (a) but as frequently the left (c) forme a semicircle at right angles to the longituinal axis of the neck (f) an, in this position, was finally carrie above the lip (e). The other lobe, which was slightly fole near its istal en (a), appeare as if to tap or "feel" an iniscernible neck bounary. Not once, even when both peristomallobes were free, was any activity of the pectinellae etecte. Relaxation an con- 231 traction of the boy continue without interruption throughout the ay. Because a slight boy secretion followe each contraction, it appeare that the peristomal lobes, functioning like a plasterer's trowel, merely carrie this material aloft an sprea it rather than prouce it themselves. Graually, the proximal portion of the extension () arkene somewhat an became clearly iscernible, but the istal portion (b) became only vaguely so. At 4:00 PM the extension, still inistinct istally, measure approximately 66p.. The organism now lay in the proximal portion of the sac. After perhaps 2 hours of "inactivity," this sessile stage metamorphose into a motile swimmer which, following three or four unsuccessful attempts, finally swam free of the originallorica leaving, as usual, the istinct green area in the proximal region of the sac which marke the ol boy attachment point. Unlike other observe swimmers, this one "crawle" slowly along the surface of the submerge glass plate. Its vermiform boy, only slightly attenuate posteriorly, measure 415p.long but only33p. wie. The following morning this swimmer was foun ea not far from the lorica whose neck ha been extene. As far as was iscernible, it ha mae no attempt to secrete a new lorica. The extension (Fig. 3) ha arkene throughout its entire length but unfortunately was fraye istally (a) an evoi of lip (a) an spiral whorls (b). Were this the only case in point, one might accept for all neck extensions Anrews ' (1923: 242) statement: While the original [lorica} is mae by an animal without lobes which then transforms into the lobe form, it seems probable that the extensions are ae by the animal when with quite ifferent anatomy at the anterior en.... If true that the perfect form can secrete spiral tube an terminal lip with out the usual special neck an mushroom shape it woul seem to follow that it is not so much one specialize part of the boy that makes the form of the welling as it is temporary contractions " an secretions ' that may be active in very ifferent parts of the boy, since the area of secretion that must. have been active in the seconary tube an

4 232 PACIFIC SCIENCE, Vol. XVIII, April fj a.. b e FIG. 3. M etafolliculina anrewsi showing : a, fraye, istal en of neck extension; b, neck extension without spiral whorls; c, lip of neck;, spiral whorl; an e, neck. lip-making is very far remove from the area originally active in the making of the first tube [neck},... [since} the arms are mae from the region very far from the anterior en of the larval swimmer. While my single observation proves that a neck :extension, even though imperfect, can be the prouct of the sessile stage it oes not exclue other extension possibilities. II. Neck Extensions by the Stage Remaining in the Lorica following Binary Fission. As previously state, the proximal portion following binary fission metamorphoses into a sessile stage, characterize by peristomal lobes. This stage persi sts uner laboratory conitions from one to several ays. This metamorphoses back into a swimmer bur there is every reason to assume that, after a perio of rest, it might unergo binary fission or inee prouce, as previously escribe, an imperfect neck extension. How ever, this is mere conjecture. III. Neck Extension by the Stage Leaving the Lorica following Binary Fission. Although this stage might possibly prouce a neck extension, it was never observe to make one. Swimmers were often observe which seeme to experience consierable ifficulty in leaving the Iorica, but finally all were able to o so. IV. Ne ck Extensions by a New Swimmer (or Swimmers ) entering Another Lorica. Lagotia viriis ( Fig. 4), with well-evelope sac (g) an neck (e), was observe trappe in its lorica by a swimmer whose attachment point ( b) wasl ocate either on or just below the wellevelope lip (c). While at first sight this stage of neck extension might seem to fall uner III ( the Stage Leaving the Lorica following Binary Fission ) such was not the case. As far as is known, L. viriis oes not make neck extensions. Although it un ergoes binary fission, the istal portion metamorphoses into a swimmer which leaves the ol lorica to start the process anew. Moreover, when first observe the anterior or pectinella e en of the swimmer pointe own into the neck an only later contracte an forme a living plug which completely close the neck ( e). During this time the entrappe folliculini lay motionless at the proximal en of the sac. As in M. anreiosi, a viscous secretion appear e just above the lip ( c). There was no apparent movement either of the swimmer or of its fuse cilia. Whereas the folliculini in the sac was a light bottle green, the swimmer attache near the lip was a eep violet. During the next 2 hours this became lighter until finally it approximate the green of the folliculini in the sac. Slowly there emerge what at first was mistaken for a proboscis. This came not from the very top of the ol lorica but rather more from the sie an extene (as illustrate) to the top of the ol sac. Not once, however,

5 Neck Extensions in Folliculinis-MATIHEWS were observe the counter clockwise movements so characteristic of normal neck formation. This was unerstanable because, although it resemble a proboscis, it alreay possesse peristomal lobes (). Believing the process complete, I mae a small aperture (h) in the lorica (g) in orer to etermine if the entrappe folliculini woul attempt to free itself. Rather more quickly than expecte, it metamorphose into a small but otherwise normal folliculini which almost immeiately gaine access to the outsie by means of this aperture (h). There was no "feeling aroun" insie the sac for the location of this opening: rather, the animal went irectly to an through it. These two folliculinis share the same lorica from March 22 to March 24. During this time the folliculini attache to the sac continue to use the aperture mae for it. It woul relax an exten its boy an peristomal lobes (f) high above the orsal surface of the ol sac but mae no effort to secrete a new neck. The folliculini attache near the ol lip (c) was at no time.20 0 JJ r a b e,--i FIG: 4. Lagotia viriis as viewe from the right sie showing: a, hemispherical, caplike neck extension; b, boy attachment point; c, lip;, peristomallobes of new occupant ; e, neck; t. per istomal lobes of original occupant; g, sac; an b, aperture cut in sac. 233 as active as the one in the ol sac. Its peristomal lobes () were never hel aloft an the beating of their pectinellae was never observe. The following morning (March 25) both folliculinis ha vacate the ol lorica. Whether or not they metamorphose into swimmers was not observe. However, the swimmer that ha attache itself near the ol lip ha secrete a strange type of neck extension (a). This consiste of a hemispherical cap whose opening was place at right angles to the main or longituinal axis of the original neck. Although it is ifficult to istinguish one species of swimmer from another, the fact that this swimmer was at first a eep violet an that Parafolliculina violaceae were present on the original plate suggests that in this instance the neck extension may possibly have been the result of another species! Because uner laboratory conitions organisms frequently respon abnormally, moifie experiments were performe in the organism's natural habitat. Empty loricae of M. anrewsi without extensions were staine with aciulate borax-carmine, washe thoroughly; an the glass plates were returne to the anchorage lagoon at Coconut Islan. At the same time, other empty unstaine lorica without extensions were marke an these glass plates were returne to the organisms' natural habitat. Although both staine an unstaine loricae were observe over a perio of 2 months, neither possesse new occupants nor extensions. An although the iscouraging results of these experiments throw some oubt on the possibility that neck extensions are forme by new swimmers entering ol loricae, other naturally occurring examples point very strongly to this possibility. In M. antrewsi the conition illustrate in Figure 5 is frequently encountere. Two boy attachment points (, e) are clearly iscernible. Although Penar (1919: 317) incorrectly assumes that longituinal fission occurs in Folliculina boltoni (see his Fig. 17), he correctly points out that only a single boy attachment point persists, that of the original occupant. If, as suggeste by Anrews, fleck extensions are the result of the original occupant of the lorica, then only a single attachment point shoul be present. It is absur to assign two attachment

6 234 points (, e) to a folliculini now known to unergo only binary fission. It is equally absur to assume that the present boy attachment point (e) permits a better peristome exit. In light of possibility I (Neck Extensions by the Stage that Secrete the Lorica), two attachment points an two neck extensions might be explaine as follows: the builer of the original lorica, once the neck (c) was complete, contracte into its sac but, after a perio of rest, instea of metamorphosing into a swimmer, relaxean, while in the lobe stage, secrete the first imperfect neck extension (b ). It then withrew an metamorphose into a swimmer which vacate the lorica. The present boy attachment point (e) is that of a new swimmer which entere, became attache, an, while in the motile stage, secrete the secon extension (a). This may explain in part why spiral whorls are absent in the first extension (b) an why c /32 J1 FIG. 5. Meta/olliculina anrewsi as viewe from the right sie showing : a, secon neck extension; b, first neck extension; c, neck;, original boy attachment point; an e, present boy attachment point. PACIFIC SCIENCE, Vol. XVIII, April 1964 they are present in the secon (a). This might also account for the fact that the iameter of the secon extension is approximately half that of the first. While these possibilities are not conclusive, other examples suggest that neck extensions may have multiple origins. Frequently M. Norgari (Fig. 6A) is observe in which the boy attachment point ( ) is far remove from the base of the lorica (e). In such instances either the boy has free itself from its original attachment point (e ) an become reattache ( ), or another swimmer has entere the ol lorica an establishe itself. Because many M. norgari with an without extensions (Fig. 6B-C) possess loricae whose lengths excee that illustrate in FigureoA an yet experience no ifficulty in extening their peristomal lobes, it seems rather unlikely that reattachment in the shorter form was the result of necessity. Moreover, if (Fig. 6A ) was the original boy attachment point there is no way, base on our present knowlege, to explain the formation of that portion of the lorica between an e. If one assumes that the lorica illustrate in Fig. 6A is not the prouct of its present occupant, how oes one explain the formation of the extensions illustrate in Fig. 6C, since only one boy attachment point (e) is present? If one rejects Anrews' theory that the present occupant (Fig. 6C) is responsible for the lorica (-e) an its extensions (c- an b-e ) then one must exten Hazi 's theory to inclue the possibility that that portion of the lorica between c- may have been secrete by a secon swimmer, an that portion between b-c by a thir. As improbable as this may at first appear, there is some evience at e (Fig. 6C) to support this view. Although it is possible that none of the original attachment-point material remains (Fig. 6A-e), occasionally (Fig. 6C- e) material accumulates whose texture an staining affinity appear ientical with those of the present boy attachment material. Surely, for those examples in which swimmers have entere ol lorica an built extensions, Hazi is correct in limiting the count of the spiral whorls to those of the original lorica an,excluing the number of whorls ae by new swimmers. However, in cases in which the

7 Neck Extensions in Folliculinis-MATIHEWS 235 builer of the origi nal lorica also as extensions this metho of counting mayor may not result in a correct whorl num ber. Alth ough these possibilities of accounting for neck extension place in question the limi te alternatives of oler theories, the process must be observe in many species before these possibilities can be accepte -unequivocally. C A e B 1.0 mm G FIG. 6. Meta/ olliculina norgari showin g: A. a, peri stornal lobes; b, boy; c, lorica;, boy attachment point; an e, base of lorica, B. a, nucl eus. C. a, peristomal lobes; b-e, secon extension; c-, first extension; an e, present boy attachm ent point. c e LITERATURE CITE D ANDREWS, E. A Folliculina: case making, anatomy an transformation. Jour. Morph., 38: DAS, S. M The biology of two species of Folliculiniae foun at Cullercoats, with a note on the British species of the family. Proc. Zool. Soc., 117: DEWEY, V. C Test secretion in two species of Folliculina. BioI. Bull., 77: FAURE-FREMIET, E. i932. Division er morphogenese chez Folliculina ampulla O. F. Miiller. Bull. BioI. France et Belg., 66: H ADZI, J Stuien tiber Follikulinier. Acaemia Scienriarum er Arrium, Slovenica Biology. 2: MATIHEWs, D. C Aitional recors of Folliculinis ( Protozoa) in H awaii. Pacif. Sci. 16( 4 ) : In press. Hawaiian recors of Folliculinis (Protozoa) from submerge woo. Pacif. Sci. PENARD, E On Folliculina boltoni ( S. Kent. Jour. Roy. Micros. Soc., Ser :