Contributions tothe Morphology, Infraciliature and Ecology of the

Europ.J. Protistol.27, 60-7 0 (1991)
March 28, 1,991,
Buropean Journal of
PROTISTOLOGY
Contributions
to the Morphology,
Infraciliature
and
Ecologyof the Planktonic
CiliatesStrombidium
pelagicumn sp., Pelagostrombidium
mirabile
(Penard,
1916)n.9.,n. comb.,and
Pelagostrombidium
fallax(Zacharias,
1896)n.9.,
n. comb.(Ciliophora,
Oligotrichida)
Karl-Heinz
Krainer
Kluckygasse,Vienna, Austria
SUMMARY
Freshwatersamplesfrom excavatedgroundwater ponds (Styria, Austria) were examined for
planktonic ciliates.Among these, the following 3 common specieswere investigatedby live
observationsand protargol impregnations:Strombidium pelagicum n.sp., Pelagostrombidium
mirabile (Penard,191,6)n.g., n. comb., andPelagostrombidiumfallax (Zacharias,1896)n.g., n.
comb. The new genus Pelagostrombidium is characterizedby a spheroidal neoformation
organelle (embryonic body) which has a winding exit canal, opening out close to the
cytopharynx. The somatic ciliature is reduced to a supraequatoriallylocated circumferential
paratene;closelyposterior to the latter is a girdle of argyrophilic granules.Pelagostrombidium
mirabile differs mainly from P. fallax in shape, cell colour and numbers of buccal adoral
membranelles.Strombidium pelagicumhas a tubelike neoformation organellewhich opensinto
the circumferential paratene. The somatic ciliature consists of an equatorially located
circumferential paratene, a ciliated girdle kinery and a longitudinally oriented, ciliated
postequatorialkinery. Abundance and biomasswere recordedover 2 annual cycles(1986/87).
Keysto the generaof the family Strombidiidaeand to the freshwaterstrombidiids are proposed.
The structure and function of the circumferential paratene and neoformation orsanelles are
discussed.
Introduction
Following the descriptionsof some planktonic Askenasla-species(Krainer and Foissner,in press),further planktonic freshwaterciliatesareto be representedin this report.
At presentthe family Strombidiidaeincludesapproximately 80 speciesin 5 genera126,27,30-321. Undoubtedly,
with the growing application of silver impregnation
techniques in the ciliate taxonomy, this number will
increasesteadily.
The majority of the species belongs to the genus
Strombidium Claparöde and Lachmann and inhabits the
marineplankton ll, 4 -6, 9, 13, 1.5, !6, 1.8,23, 26, 27, 29,
0932-47
39l91I 0027-0060S3.50/0
31,32,361. Only 7 speciesthat live in freshwaterhabitats
h a v es o f a r b e e nl i s t e d[ 3 , 1 1 , 2 4 , 2 5 , 3 0 , 3 3 , 3 4 , 3 5 , 3 7 , 3 8 ,
39, 41). The role of these ciliates in the planktonic food
web is considerable, a reddish-brown discoloration of
shorewater by StrombidiwmreticwlatumandTintinnopsis
beroidea,recentlyobservedin southernNorway, confirms
this view [10]. In connectionwith this it was pointed out
repeatedlythat the taxonomy of the strombidiids ought to
be given an extensiverevision, in order to reduceerrors in
speciesdetermination18,2Tl.In spiteof theserequests,rhe
taxonomy of the strombidiids still leavesa great deal to be
desired. Noticeably little is known on the freshwarer
strombidiids. As far as I know, silver impregnations and
O 1991 by Gustav Fischer Verlag, Stuttgart
Strombidiids' 61
of Freshwater
Descriptions
examinations by electron microscopy have been carried
out on freshwater species only once t371. This paper is a
first attempt to give adequate descriptions of 3 common
freshwatei sp.cies by uiing silver impregnation techprocedures usually
niques. Fixaiives and i-prögttation
damage seriously the strombidiids. Therefore it is necessary to Äake detaiied examinations of the living material, but
tiris is difficult because of easily bursting individuals. It is
my wish to take part in bridging the great gap between
spä.se ta"ottomiC works on the one hand and the large
amount of ecoloeical works on the other.
Material
and Methods
The specieswere collected from the plankton of 2 eutrophified,
excavatädgroundwater ponds (eachsome 8 ha).in the Leibnitzer
Feld (Sryriä,Austria: E 75",32'; N 46", 49'). The water column
was samplified at 2 depths (1 m: surface layer; 3 m: sediment
Iayer).Sampleswere taken once a fortnight from March 1986 to
Tune 1987 with a 5 liter "schindler" sampler. Subsampleswere
iixed in the field using HgCl2 and Bouin's fixative, subsamplesfor
counts were additionaily stained with about 10 drops of a
solution ol 0.04% bromophenol blue [2]. Specimens were
examinedin vivo and in protargol impregnatedslides[20]. Note
that this staining method generallycausesa shrinkage-of the cells
of about 2046%. The drawings of the impregnated specimens
were made with the help of a cameralucida.'Wherepossible,the
neotypeindividual was usedfor preparing the figures;otherwise,
compösite drawings were made. All measurementswere performed at a I2}b-fold magnification. Statistical procedures
follow methodsdescribedin Sokaland Rohlf [40]. Subsamplesfor
estimatingthe number of individuals were sedimentedovernight.
Counts were carried out on slides at a 100-fold magnification.
Abundance is expressed as cells/liter. The gross biomass,
expressedas mg/m3,was calculatedfrom.protargol preparations
by using the eitimated cell volume,(reducing the complicated
shapeto simple geometric figure and assuminga specific graviry
"
the abundance.Holotype-, paratyqe-a!d
of i.01, multipliedwith
neotype-slideiof eachspeciesdescribedhas beendeposited.in.the
collection of microscope slides of the Oberösterreichischen
Landesmuseumin Linz, Austria.
Results
Proposed Characterization of the Family
Strombidiidae
Free-swimming and predominantly planktonic forms
both in marine and freshwater habitats. Posterior cortex
usually stiffened up with polysaccharid plates, formlng a
"lorica" which is coveredwith a perilemma 18,1'4,18,24,
37]. Extrusomes needle-like,located in plasma pockets'
circumferentially arranged 124, 26, 27, 32, 33, 34, 371.
Bacteri-, algi- and carnivorous. Chloroplast sequestration
well documentedfor both marine and freshwater species
127,29,37]. Restingcysts with anterior micropyle and
äperculum [e, rc| Tidal rhythm observed [16]. Several
specieswith ecto- and endosymbionts [8, 27]. Somatic
cilirture mostly reducedor even completely absent.Deep
buccal cavity with undulating paroral membrane at its
right border,usually encircledby peristomialcollar-Apical
ciiclet of membranellesroughlv forming number "9", with
2 distinguishableparts: t) ö[är adorafmembranellesand
II) buccal adoral membranelles.Membranelles in several
speciesmodified to specialized cilia with thigmotactic
function U.5, LTl.Bipartition enantiotropic [17]' Coniugation by fusion at buical membranelles.New oral ciliature
for the opisthe developswithin characteristicneoformation organelles.
lllwstrated Key to the Genera of the Family
Strombidiidae
with Montagnes et al- [32],
Taxonomic remarhs.I agree
who restored the genus Laboea Lohmann as a well
charucterized,valid taxon. In this key, the genusBuehringa
Busch is also restored as a valid taxon. Maeda and Carey
[27] dissolved the genera Laboea and Bwehringa in theit
ieviiw and placed its members into Strombidium Clapatöde and Lachmann. The genus Parastrombidium Fau6Fremiet is an insufficiently described genus with no
type-specieserectedand thereforenot included in this key
(Fig.6).
1 - Posterior cortex stiffened up with polysaccharid
....2
plates,formingdistinctlorica.
- Cortex without polysaccharidplates' instead a heterogeneously retitulated cytoplasm. Body globularMäcronucleus horseshoe-shaped.Freshwater and
...Metastrombidiwm Faur6-Fremiet'
marine
(Fis.8).
1.924
2 - Multiplemacronuclei....
.....' 3
- Singlemacronucleushighly variable in shape; sometimäs up to ahalf-dozensegments(probably postcon..... 4
jugants)
3 - Mäcronuclear segmentsconnectedto each other like
a string of beads. Characteristic contractile tail
originating from dorso-posterior area. Marine
..Tontonia Faur6-Fremiet,191'4(Fig.a).
- Macronuclear segments scattered throughout the
cytoplasm. No spine. Lorica with 3-6 oblique
whorls, forming sinistralhelix. Marine ..... .... Laboea Lohmann, 1908 (Syn. Conocylls Meunier,
1907;'Woodania Leegaard, 1915 (Fig. 7)).
4 - Presenceof 2 differenttypesof polysaccharideplates;
anterior platesrectangular,posterior platespolygon....Bwehringa Busch, 1'921'
al. Marine
(Fig.s).
- Preienceof one type of polysaccharidplates, usually
.......5
polygonalinshape
5 - Macronucleus (MA) from sphericalto drop-shaped,
usually occupying the region below the buccal membraneile fiela (BAM). Neoformation organelle consisting of a spheroidal embryonic body (EB) and-a
winding exit canal (EC) which opens close to the
cytopharynx. Circumferential paratene (CP) supra..Pelago'
equalorially located. Freshwater
strombidium n.g. (Figs.1,2).
- Macronucleusmore or lessspherical,usually centrally located. Neoformation organelle tubelike which
opens into the circumferential paratene' the latter
usually equatorially located. Freshwaterand marine
. . . . . . . . . - S t r o m b i d ' i u nC l a p a r ö d ea n d L a c h m a n n ,
1 8 5 9 ( F i g .3 ) .
62 . K.-H. Krainer
Figs. 1-8. Genera of the Strombidiidae
(from severalsources).- Fig. 1. Schematic
figure of Pelagostrombidium. - Fig.2.
Magnified detail of Pelagostrombidium
showing peristomial collar (PC), collar
membranelles(CAM), intermembranellar
ridges (IR), extrusome bundles (EX) with
an ejected state and circumferential paratene (CP): detail shows hypothetical pattern of kinetids. - Fig. 3. Schematicfigure
of Strombidium. *Fig. 4. TontoniaFauftFremiet, I9I4. -Fig. 5. BuehringaBusch,
192I. - Fig.6. Parastrombidium Faur6Fremiet, 1924. - F ig. 7 . Lab oea Lohmann.
1908. - Fig.8. Metastrombidium Faw6Fremiet, 1924. BAM:
buccal adoral
membranelles; CAM :
collar adoral
membranelles; CP : circumferential paratene; EX : extrusomes; 6Q : girdle of
argyrophilic granules; Ql( : girdle kinety;
IR : intermembranellarridges; L : lorica; MA : macronucleus;MI : micronucleus; NO : neoformation organelle;
pQ : peristomial collar; PK : postequatorial kinety; p1y : paroral membrane.
Descriptions of Species
Strombidiwm Claparöde and Lachmann, 1859. Syn.
StrombidionCl. and L., 1859 (par lapsus;[21]).
Proposed diagnosis (Fig. 3). Shapeovoid to long fusiform, in severalspeciesposterior elongations.Extrusomes
wedge-shapedbundled, forming funnel-like arrangement.
Collar adoral membranelles (CAM) and buccal adoral
membranelles (BAM) usually merge with each other.
Somatic ciliature consists of (i) a roughly equatorially
located circumferentialparatene(CP), (ii) a ciliated girdle
kinety (GK) and (iii) a longitudinally oriented, ciliated
postequatorialkinety (PK). Neoformation organelle(NO)
a tube closed at one end which ooens into the circumferential paratene.
Strombidiwm p elagicum n.sp.
Diagnosis. Sizein vivo 40-60 x 30-45 pm. 16 collar
membranelles.Buccal lip conspicuous.Lorica with longitudinal indentation.
Type location Excavatedgroundwater ponds near Graz
(Styria, Austria).
Deriuatio nominis. "pelagicum" refers to the preferred
habitat, in which the speciesoccurs.
Description (Figs. 28-32, 48-55; Table 1). Shape
ovoid, round in cross-section,widest at equator, posteriorly attenuated(Fig. 28). Macronucleus round to irregularly outlined, with large chromatin bodies, occasionally
with huge central nucleolus. Two spherical micronuclei
lying closelybelow macronucleus(Figs.28, 53). Contractile vacuole not observed. Lorica with indentation that
extendshalfway lengthwisefrom posterior pole to circumferential paratene (Figs. 28, 30, 31). Extrusomes (EX) in
vivo 16-23 pm long, arranged in numerous bundles.
Bundles extend internally tapering to a point posteriad
(Figs. 28, 30). Cytoplasm contains numerous colourful
granules giving the cell a greenish-grey to reddish-brown
colour. Locomotion restless.Tube of neoformation organelle (NO) circular in cross-section,becoming narrower
toward opening; wall of posterior closed portion irregularly granulated, wall of anterior narrower portion (exit
canal,EC) non-granulated(Figs.29,31",54). New membranellesfor the opisthe start developing in region between
granulated portion and exit canal (Fig. 55). Collar membranelles(CAM) arisebetweendistinct indentations,inrerconnectedby transverseand curved fibres (TF, Figs. 28,
31), basescomposed of 3 polykinetids of equal length.
Buccal membranelles(BAM) composedof 3 polykinetids
each,posteriormost of each baseup to 617 the length of the
others. Paroral membrane (PM) composedof 2-3 rows of
single-filedbasalbodies,coveredby buccallip of peristom-
Descriptionsof FreshwaterStrombidiids' 63
Table 1. Morphometry of Strombidium pelagicwm. All data
basedon protargol-impregnatedspecimens
Character
r
44.0
Body, length
32.7
Bodv. width
14.6
Maironucleus, Ionger axis
12.4
Macronucleus. shorter axis
2.3
Micronucleus. diameter
2.0
No. micronuclei
16.0
No. collar membranelles
10.8
No. buccal membranelles
Field of buccal membranelles, 13.8
length
5.0
Circumferentialparatene,
width
Distance from posterior mar- 24.2
gin of circumfuential paratene
to posterlor pole
Postequatorialkinety, no. of 12.6
dikinetids
SD
CV
Min Max
6.6
5.3
3.3
2.3
0.2
0.0
0.0
2.5
3.8
15.0
16.3
22.7
18.8
7.7
0.0
0.0
23.t
27.5
36 54
26 3 8
22
8
18
9
2
3
2
2
16 L6
1.6
8
1.L 22
0.9
18.6
3
6
6.3
25.9 18
4l
5.0
39.7
22
8
All measurementsin pm. Legend: CV : coefficient of variation in
"/o'.Max: maximum; Min: minimum; SD: standard deviation; x : arithmetic mean.
Figs.9-19. Strombidiumuiride.- Fig.9.
Afler Roux [38]. - Figs.10, 13. After
Penard[34].- Fig. 10.Ventralview.Note
- Fig. 13.Bipartiorganelle.
neoformation
tion. - Figs.Il, t2, L4. AfterKahl [24].
All ventralviews.Note extrusomebundles
(11,
('1,1,
organelles
t2, 14),neoformation
plates(11, 12). 14) and polysaccharid
Figs.15-17. After Borror [5, 6]. Note
girdlekinery(15).- Fig.18.AfterDragesco [13]. - Fig.I9. After Lokot [251.
Figs.20-24. Pelagostrombidiummira'
bile. - Figs.20-23. After Penard[33].Figs.20, 22. Yentral views, showing
andneoformamacronucleus,
extrusomes
- Fig.21. Coniugation.
tion organelles.
Conjugants with well developed new
within neoformationorgamembranelles
nelle. - Fig.23. Bipartition.- Fig.24.
bundles
AfterLokot [25].Noteextrusome
neoformation organelle.
and
Figs.25-27. Pelagostrombidiumfallax
after Sebestfen[39]. - Fig.25. Dorsal
view. - Fig.26. Ventral view. - Fig.27.
Different form.
ial collar (Figs. 31, 32). Circumferential paratene (CP)
4-7 p,m wide, with a small gap suborally, composed of
numerous oblique, argyrophilic rods and weaker impregnated meshes inbefween, the latter possibly enclosing
pores (Figs.30, 31,49). Girdle kinety (GK) composedof
numerous dikinetids bearing clavate cilia of approximately
2 pm in length by 1 pm apart (Figs.28, 30,50). Postequatorial kinety (PK) composed of dikinetids, its number
varying (possibly correlated with cell size); usually with
some 3 pm long pointed cilia at each anterior basal body;
extends from posterior pole a third part of cell length
anteriorly (Figs.28, 30, 31, 51, 55).
Abundance and biomass.Achievedhighestnumbers on
August 17,1986with740 cells/literand 18.5 mglm3 at.a
depth of 1 m, and 258 cells/literand 6.5 mg/m3at a depth
of 3 m. Lower numbers observed in November 1986,
December1986,April 1987 and June 1.987,not exceeding
200 cells/liter.
Comparison with other species.Strombidium ui'rides.I.
seemsto be a conglomeration of several species(Figs.
9 -1.9; 13,4, 1.1.,13, 24, 25, 27, 34, 371) : S. uiride sensrt
PenardI34l has 10-11 collar membranelles.Kahl [24], for
W'
64 . K.-H. Krainer
his part, differentiated 3 forms: a large conical form
(around 80 pm), which has 12 collar membranellesand
lives between litoral submerse vegetation (Fig. 1I) and 2
smaller forms (40-60 pm) which inhabit the plankton
(forma pelagica; Figs. 12, 14). The marine forms sensu
Borror [4] and Dragesco [13] have 22 (number probably
includes BAM-membranelles) and 17-L9 collar membranelles,respectively(Figs. 15-18). I did not find a species
which correspondsexactly to any of the availabledescriptions of S. uiride, but observedone which has constantly
1.6 collar membranelles, a conspicuous buccal lip and a
longitudinal lorica indentation. It mostly resemblesS. yiride f. pelagicd sensu Kahl l24l but he indicated only 12
collar membranellesin his drawings (Figs. 1,2,1,4).Therefore I think it was wise to establisha new species.
Pelagostrombidium n.g.
Diagnosis (Figs.1, 2). Roughly gyroscope-shaped.
Contractile vacuole absent.Extrusomes(EX) arrangedin few
wedge-shaped bundles. Collar adoral membranelles
(CAM) and buccal adoral membranelles(BAM) arranged
in a way that the latter begin distinctly inside the former.
Somatic ciliature reduced to a supraequatoriallylocated
circumferentialparatene (CP); closelyposterior is a girdle
of argyrophilic granules (GG; to date I am not able to
decide whether the granules are basal bodies or not),
enclosing lower portion of buccal adoral membranelles.
Neoformation organelle comprisesembryonic body (EB)
and exit canal (EC) which opens close to the cytopharynx.
Type-species. Pelagostrombidium mirabile (Penard,
1 9 1 6 )n . c o m b .
Deriuatio nominis. The genus name refers to the pelagic
habitat in which the 2 members of this genus occur
characteristically.Neuter gender.
Pelagostrombidiwmmirabile (Penard, 1916) n. comb.
(basionym. Strom b i dium mir a b il e P enard, 19 t 6)
Redescriptioz (Figs. 20-24, 33-39, 56-59; Table 2).
Sizein vivo 3 0-65 x 25 -50 pm 124,25, 33l. Shapeslender
conical to ovoid. Anterior third round in cross-section.
pelagicwm,
Figs.28-32. Strombidium
from life (28) and protargol-impregnated
specimens(30-32). Fig.29 aker Penard
1341..- Fig.28. Ventral view, showing
nuclear apparatus,extrusomes,penstomial collar and apical membranelles. Fig. 29 . Neoformation organelle o{ S. uiride. - Fig.30. Dorsal view. - Fig.31.
Ventral view. - Fig.32. Anterior view.
BAM : buccal adoral membranelles;
CAM:
collar adoral membranelles;
CP : circumferential paratene; EC : exit
canal of neoformation organelle; EX :
extrusomes; 611 : girdle kinety; L : lorica; LP : polysaccharid plates; NO :
granulated sac of neoformation organelle;
OM : oral membranellesfor the opisthe;
PK: postequatorialkinety; PM = paroral membrane; TF : transversal fibres.
Scales: 10 pm (x 1200).
. 65
Descriptions
of Freshwater
Strombidiids
posterior two thirds slightly compresseddorsoventrally.
Apicalpolewith narrow peristomialcollar (Figs.20,22,
24,33).Macronucleus
from spheroidto club-shaped,
with
nuclear envelope,filled with medium-sizedchromatin
of
bodies.Micronucleuselliptical,locatedin depression
plates
macronucleus(Figs.24, 33, 59). Polysaccharid
(in
2-4 pm in size,from hexagonal[33] to square-shaped
Styrian populations; Fig.33). Extrusomes in vivo
1,4-1.8pm long, ejectedstates80-90 pm long, having
barbsdistally(Fig.2). Usually2 bundlesventrallyand2-4
bundlesdorsally, accordingto Penard[33] only 2 large
bundlesin all (Figs.20,22,24, 33). Cytoplasmcontains
tightly packedcolourful granules2-4 pm in size,symbiotic green algae as well as very small granules("cell
semoline"l[24, 331).Swimsvery quicklyin shortspirals.
Collar membranelles(CAM) occasionallymodified to
fibres
by transversal
thigmotacticcilia[33],interconnected
at their posteriormostends:each basecomposedof 3
polykineiids
of equallength'(Fig.
39).Buccalcavitywith
paroralmembrane(PM) at its right border;atleft,l.2-1.5
(BAM),eachcomposed
of 3 polykibuccalmembranelles
netids,anteriormostof eachbaseup to 617thelengthof the
others (Fig.39). Argyrophilic oral fibres derive from
Figs.33-39. Pelagostrombidiwm mirabile, from life (33, 34,37) and protargolimpregnated specimens(35, 36, 38, 39).
Fig.37 after Penard [33]. - Fig. 33. Ventral view, showing nuclear apparatus,
extrusomes, peristomial collar and apical
membranelles.- Fig.34. Extrusome. Figs.35-37. Neoformation organelles:interphasestage(35. 37); progressivestage
of development (36). - Fig. 38. Ventral
view. - Fig. 39. Oblique anterior view.
BAM : buccal adoral membranelles;
CAM:
collar adoral membranelles;
CP = circumferential paratene; EC : exit
canal of neoformation organelle; GG =
girdle of argyrophilic granules; L : lorica;
OM : oral membranelles for the opisthe;
PP[ : paroral membrane;UF : U-shaped
buccal fibres. Scales: 10 pm (x 1200).
posterior buccalmembranelles,
extendinginternally and
coil upwards.ProminentU-shapedbuccal fibres (UF;
Fig.39). Circumferentialparatene(CP) 2-4 pm wide,
(Figs.33, 38,
interruptedin regionof buccalmembranelles
56). Girdle of argyrophilicgranules(GG) consistingof
pairedor tripled granules;granulesseparated
from each
otherby long,stiff fibres(onlyseenin vivo; Figs.33, 56).
Embryonicbody (EB)in vivo greyish-blue,
its integument
granules;
interspersed
with argyrophilicdumbbell-shaped
penetrates
integumentat right
exit canal(EC)colourless,
side,winds aroundtwice beforeleavingembryonicbody
(Figs. 22, 24, 35, 37). Elongatedduring bipartition,
forminga moreor lesscucumber-shaped
cavity(Figs.20,
21,33,36).
Abwndance
and biomass.
Very abundantthroughoutall
seasons
with highestpeaksreachedin the winter months.
Most numerouson 10 November, 1986 with 5100
cells/literand 50.6 mdm3 at a depth of 3 m, on 25
November, 1986 6200 cells/liter and 61.5 mglm3 at a
depth of 3 m. Also numerousin May 1986 with 400
cells/literand 3.7 mdm3, in August 1.986with 1.31.6
cells/literand 13 mdm3, in December1.986with 1275
66 . K.-H. Krainer
cells/liter and 1.2.6mdm3, in January 1.987with 161.2 (Figs.40, 42, 43-45). Cytoplasm contains some oildropcells/liter and 1.6mdm3 and in Ap_iI 1.987with 2202 like inclusions,tightly packedreddish-browngranules,the
latter bunched together at equator eccentrically(Figs.40,
cells/literand 21.3 mg/m3.
Pelagostrombidiumfallax (Zacharias,1,896)n. comb.
(basionym.Psilotrichafallax Zacharias,1896)Syn.
Strombi diwm fallax (Zacharias,"1.89
6) Kahl, 1933
41, 43-45). Granules give the cell characteristic rich
reddish colour. Food vacuolescontain diatoms and peridinees[24]. Embryonic body (EB) reniform, mostly in pairs
(Fig. a0). Collar membranellebases(CAM) composedof 3
polykinetids each,left polykinetid of eachbaseup to 9ll0
the length of the others (Figs.46, 47).Buccal cavity wide
and deep; paroral membrane conspicuous, at its right
border; atleft,1.9-22 buccal membranelles(BAM) extend
at leasthalf the cell length internally; basescomposedof 3
polykinetids each,anteriormost of eachbaseup to 617 the
length of the others (Fig. an. Prominent U-shapedbuccal
fibres (UF; Fig.46). Circumferential paratene (CP)
2-4 1tm wide, interrupted in region of buccal membranelles(Figs.40, 4 6, 47, 62). Girdle of argyrophilic granules
(GG) consistingof single granules (Fig. a0).
Redescriptioz(Figs.2527, 40-47, 60-62; Table2).
Sizein vivo 43-90 pm x 40-80 trrm.Shapevariable,from
conicalto almostglobular,mostlyasdepictedin Figs.43,
44 (Figs.25--27,40, 41.,43-4 5). Dorsalsideprominently,
ventral side slightly arched.At anterior pole narrow
peristomialcollar with broad buccallip (Fig.40). Intermembranellar
ridges(IR)hyaline,lyingcloseto eachcollar
(possiblystriae,cp. [7]), givethe impression
membranelle
originatein deepindentations
thatthecollarmembranelles
(Figs.2, 40,43-45).Macronucleus
with nuclearenvelope,
containsirregularlyoutlinedchromatinbodies.Micronuplatespolygoncleuselliptical(Figs.27,40).Polysaccharid
Taxonomic remarks. The original description of P. falal, forming cauldron-to eggcup-shaped
lorica (Figs.40, lax is v ery incomplete ( [a 1] ; Fig. 4 1). There are, however, a
46, 47). Extrusomesin vivo 15-20 pm long, distally few characteristicswhich support my identification. First,
knobbed,number and arrangementof bundlesvarying Zacharias mentioned that the oeristomial field extends
Figs. 40-47. Pelagostrombidium fallax,
from life (40-45) and protargol-impregnated specimens (46, 47). Fig.4l after
Zacharias 1411. - Figs. 40, 41. Ventral
views, showing nuclear apparatus, polysaccharid plates, peristomial collar and
apical membranelles. - Figs.43-45.
Shape variations and variation of extrusome arrangement. Note the intermembranellar ridges (arrows). Dotted areas
indicate food granule concentrations.Fig.46. Ventral view. - Fig. 47. Oblique
anterior view. BAM:
buccal adoral
membranelles; CAM:
collar adoral
membranelles;CP : circumferential paratene;EX : extrusomes;6Q : girdle of
argyrophilic granules; IR : intermembranellar ridges; L : lorica; NO : neoformation organelle; PM : paroral membrane; UF:
U-shaped buccal fibres.
Scales: l0 um (x 1200).
68 ' K.-H. Krainer
Figs.48-62. Protargol-impregnatedspecimens.All bars indicate 1_0trrm.- Figs.48-55. Strombidium.pelagicum.-- Fig. 48. Ventral
-Fig.49. Detail of circumferentialparatene.
viäw. Arrows indicaä circumierential parateneand kinety girdle (lower arrowheads).
j0.
Postequatorialklnety fr9.mlateral view.
Fig..51.
cilia.
girdle
Ngte
clavate
of
(arrowhead).
Detail
Fig.
Note kinety girdle
\!nety.
- Fig. 53. Optical
Note poinieä cilia. - Fig. 52. Anteiior view showlng collar ICAV; and b_uccaladoral membranelles(BAM).
longitudinal section shoi'ing macro- (MA) and micrönucleus (MI): - Fig. 54. Posterior.granulalgd.sac of neoformation organelle
(ariow). - Fig. 55. Lateral view showing progressivestageof new developingmembranelles(NM) for the opisthe. Arrows.indicate
post.quatoriil kinety. - Figs. 56-59. Pelagoslrombidiummirabile. - Fig. 56. Ventral view showing circumferentialparatene(arrows)
showing circumferential
ä"a girat. of argyrophilic"granules(GG): - Fig.57. Anterior view. --Fig.58. Optical transverse^section
p"."i.r. 1"tto*Jj. -'Fig. 59. Opticai longitudiial section showin_gmacronucleus.(ryA).. - Figs. 60-62. Pelagostrombidiumfallax.
adoral membranelles(BAM). - Fig. 62. Magnified
hlg. OO.Dorsal viäw. - Fig. 61. Ventrolateäl view showing collar (CAM) and_buccal
(CP).
paratene
indicate
circumferential
deiail of collar membranelles.Arrows
the same nature as the perizonal zone of C. medusula ot
the equatorial girdle of S. swlcatwm (cp. Fig. 2). The
circumferential paratene seemsto be widespread in the
strombidiids, but very often overlooked becauseof poorly
resolvingprotargol impregnations.
Secondly,a remarkable diagnostic feature is the cytoplasmatic neoformation organelle,within which the apokinetal stomatogenesisof the oral membranellesoccurs [8,
33,341. Penard [33] has already pointed out that Pelagostrombidium mirabile, in comparison with S. uiride, has
quite a different organelle(. . . "la structureestabsolument
diff6rente"). However, both types have odd exit canalsof
unknown function. ln L925, Dogiel [12] published the
sexualprocesses,among others, for Cycloposthium bipalmatum (Ophryoscolecidae,Entodiniomorphida), during
which he observedorganelleswhich strongly resemblethe
Descriptionsof FreshwaterStrombidiids ' 67
near to the posteriorend. Second,he noticedthat the
ventral sideis slightly and the dorsal side prominently
arched.The size(80 ptm)alsoagreesratherwell with my
measurements(Table2). SebestyenI39l describeda
Strombidiwmsp. from Lake Balaton (Hungary; Figs.
25-27), the feäturesof which correspondwell with
P. fallax from Styrianpopulations.
Table 2. Morphometry of Pelagostrombidium mirabile (uppet
line) andPelagostrombidiumfallax(lowerline). All data basedon
specimens
protargol-impregnated
and biomass.Highestnumberson27 May,
Abundance
1986 with 876 cells/literand21.3mdm3at a depthof 3 m
and on 17 August, 1987 with t776 cellslliter and
43.3m{m3 at a depthof 1 m.
Body, width
Body, length
39.4 1 0 . 3 2 6 . 1 2 6
48.0 7.1 t4.7 39
3 1 . 1 8.1 26.2 19
44.9 5 . 8 1 3 . 0 3 8
54
64
Macronucleus,longer axis
19.6
21.4
3.8 19.4 13
3.0 14.2 17
43
59
24
26
Macronucleus,shorter axis
I0.9
t2.4
2.t 1.8.9 8
2.6 20.9 \L
1,4
18
Micronucleus, longer axis
5.8
3
4
7
6
0.6 15.2 4
0.5 t4.9 2
I4.9
0.3 2.2 t4
1.5.2 0 . 4 2 . 6 1 5
I3.1
0.5 4.3 12
20.8 0.8 3.7 t9
5
4
15
22
Field of buccal membranelles, 17.5
26.4
length
2.3 r2.9 L4
2.2 8.3 24
20
30
Embryonic body, Iong axis
6.6
7.4
1.0 15.3
3.2 23.1
4.7
5.8
0.9 18.8 4
1.0 r7.4 5
5.3
Micronucleus, shorter axis
1 - Buccal membranelles (BAM) eccentrically located;
merge with collar membranelles,or bent in a right
....2
a n g l e t oc o l l a r m e m b r a n e l l e s
- Bulcal membranelles (BAM) not eccentrically
located; extend distinctly internally. Extrusomes
arranged in few bundles. Neoformation o-rganelle
consistingof spheroidalembryonic body and slender
exit canal,opening closeto the cytopharynx' Somatic
ciliature reduced to supraequatorially located, circumferential paratene. . . . .. Pelagostrombidiwm,3
2 - Collar membranelles (CAM) and buccal membranelles (BAM) merge with each other. Extrusome
bundlesnumerous, radially arranged.Neoformation
organelle tubelike, opens into circumferential par,ateie, the latter equatorially to subequatorially
located. Somatic ciliature consistsof circumequatorial girdle kinety and longitudinal postequatorial
.Strombidiwm,4
kinety .
- Buccal membranellesbent in a right angle to collar
Somembranelles.Macronucleus horseshoe-shaped.
matic ciliature absent.Insufficiently describedspecies
. . Metastrombidium nigrum l30l
3 - Shapeslenderconical to ovoid, size45 x 30 pm, cell
colour greenish-greyto orange-yellow.Polysaccharid
platesusually square-shaped.12-15 buccal membranelles extending a third of cell length internally
..P. mirabile
- Shapeplump conical to almost globular, 60 x 5O pm
in siz4 colöur rich reddish brown. Polysaccharid
plates polygonal. 19-22 buccal membranelles
äxtending al least half cell length internally
..P. fallax
4 - Shape usually ovoid. Length 40-60 pm. 16 collar
m e m b r a n e l l e. .s. . . . . . . 5 . p e l a g i c w m
- Shape usually conical. Length 70-90 pm' 10-12
..S.uiride sensu Kahl
collär membranelles
Penard
and
[34]
[24]
Min Max
x
Key to the Freshwater Species
Strornbidiwm uelox Beardsley, 1'902, and Strombidium
RlobosumFromentel, 1.874ought to be transferredto the
Strobilidiwm Schewiakoff, 1'892' Strombidiwm twräenus
"bo
Claparide and Lachmann, 1858, was transferredfrom
Kahl t24l to the genus Strombidinopsls Kent, 1881.
SD
CV
Character
No. collar membranelles
No. buccal membranelles
Embryonic body, short axis
1.r t8.4
0.8 t5.7
4.0
3.4
6
6
15
I6
8
l-)
5
7
All measurementsin pm. Legend:CV : coefficientof variation in
%l Max : maximum; Min: minimum; SD - standard deviation; x : arithmetic mean.
Discussion
Despite their important role as indicators of water
quality, information on the taxa of freshwater strombidiids is very fragmentary. Only one study has been
conducted using silver staining and electron microscopy
[37]. Therefore,many conclusionsanticipatedhereremain
at a very hypothetical stage.
Firstlv. little attention has beenpaid to the circumferential paräiene. In an ultrastructuräl study on the marine
speciesStrombidium sulcatum, Faur6-Fremietand Ganier
[18] discovereda highly differentiated somatic ciliature
(ceinturedquatoriale)made up of shortenedrows of paired
basal bodies,which have stubby cilia. SEM-observations,
likewise on marine species,revealed a structure in the
equatorial region which is interspersedwith regularly
arranged bumps. The authors interpreted this girdle-like
structure as a "hexagonally patterned arcay of trichites"
[32]. Finally, the perizonal zone of the heterotrichid ciliate
Caenomorphamedusulastrongly resemblesthe circumferential paratene of Strombidium pelagicum.Itis made up of
oblique rows of paired basal bodies, which have kinetodesmal fibres. I hypothesize that the circumferential
parateneof the speciesdescribedhere is also very likely of
68 . K.-H. Krainer
Figs.48-62. Protargol-impregnatedspecimens.All bars indicate 10 pm. - Figs.48-55. Strombidium pelagicwm.- Fig. 48. Ventral
view. Arrows indicate circumferentialparateneand kinety girdle (lower arrowheads).-Fig.49. Detail of circumferentialparatene.
Note kinety girdle (arrowhead).- Fig. 50. Detail of girdle kinety. Note clavatecilia. - Fig. 51. Postequatorialkinety from lateral view.
Note pointed cilia. - Fig. 52. Anterior view showing collar (CAM) and buccal adoral membranelles(BAM). - Fig. 53. Optical
longitudinal section showing macro- (MA) and micronucleus (MI). - Fig. 54. Posterior granulated sac of neoformation organelle
(arrow). - Fig. 55. Lateral view showing progressivestageof new developingmembranelles(NM) for the opisthe. Arrows indicate
postequatorialkinery. - Figs. 55-59. Pelagostrombidiummirabile. - Fig. 56. Ventral view showing circumferentialparatene(arrows)
and girdle of argyrophilic granules (GG). - Fig. 57. Anterior view. - Fig. 58. Optical transversesection showing circumferential
paratene (arrows). - Fig.59. Optical longitudinal section showing macronucleus(MA). -Figs.60-62. Pelagostrombidiumfallax.
Fig. 60. Dorsalview. - Fig. 61. Ventrolateralview showing collar (CAM) and buccaladoral membranelles(BAM). - Fig. 62. Magnified
detail of collar membranelles.Arrows indicate circumferentialparatene (CP).
the same nature as the Derizonalzone of C. medusula or
the equatorial girdle of S. sulcatum (cp. Fig. 2). The
circumferential paratene seemsto be widespread in the
strombidiids, but very often overlooked becauseof poorly
resolvi ng protargol impregnations.
Secondly,a remarkable diagnostic feature is the cytoplasmatic neoformation organelle,within which the apokinetal stomatogenesis
of the oral membranellesoccurs [8,
33,341. Penard [33] has aheadypointed out that Pelagostrombidiwm mirabile, in comparison with S. uiride, has
quite a different organelle(. . . "la structureestabsolument
diff6rente"). However. both tvoes have odd exit canalsof
unknown function. In 1925, bogiel [12] published the
sexualprocesses)among others, for Cycloposthiwmbipalmatum (Ophryoscolecidae,Entodiniomorphida), during
which he observedorganelleswhich strongly resemblethe
Descriptionsof FreshwaterStrombidiids . 69
neoformation organellesof Pelagostrombidiwm.Curiously enough, he observedmigrating pronuclei with tail-like
appendageswithin the cytoplasm of conjugating cells
which he likened to flagellae of spermatozoons.I believe
that this is very likely an erroneousinterpretation. Most
possibly the long appendagesare part of a limp canal
which Dogiel has overlooked. I propose the hypothesis
that the exit canals have a special function during the
conjugation process: within the canals the micronuclei
migrate from one conjugant to the other. In this case, a
closer relationshio of the familv Strombidiidae to the
Entodiniomorphiäa should be taLen into consideration.
Thirdlv. there are many contradictory observations
.oncerniäg the contractile vacuole of ihe freshwater
strombidiids. Kahl [24] noticed that the latter lack a
conventional contractile vacuole. He assumed that the
neoformation organellescould, in order to compensatethe
absence,additionally serve as osmoregulators. Almost
certainly Pelagostrombidium lacks a contractile vacuole
(Penard[33] observedover 200 specimenswithout finding
one).Strombidiwm uiride has allegedly a single contractile
vacuole, but there are only 2 observations of doubtful
value which corroborate this assumption[37,38]. Penard
[34] as well as Kahl Qal were not able to find a single
contractile vacuole. However, the two authors observed
severaloften disappearingvesiclesin the equatorial region:
usually one vesicle between every pair of extrusome
bundles.This leadsto the conclusionthat there is possibly
an unknown drainageorganelle.Maybe Penard'sequatorial ring-canalservesas an osmoregulatorand the paratene
poresmight function asopeningsfor it. However, I was not
able to verify an equatorial ring-canal by life observations
or by protargol impregnations in S. pelagicwm. On the
other hand, much indicatesthat the paratenepores might
act as "launching openings" for the extrusomes,through
which the ejectedthreads can pass (cp. Fig. 2). So far, not
enough is understood to draw any firm conclusion.
Therefore, further investigations are certainly worthwile.
Acknowledgements
This study is part of a doctoralthesisundertakenat the
Universityof Graz(Austria)and guidedby Univ.Doz.Dr. Hans
Sampl.His continuinginterestin my work is gratefullyacknowwho
ledged.Specialthanksto Univ. Prof.Dr. WilhelmFoissner,
to me and to Mag. Hubert
madehis privatelibrary accessible
I would furtherlikä to thank
Blattererför constructivädiscussion.
Dr. Markus Knoflacher,who made the equipmentof the
Institute(Graz,Austria)availableto me.
JoanneumResearch
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,