On temporal variation in the rotifer Keratella cochlearis (Gosse): the question of"Lauterborn-cycles"

Wolfgang HofmannAbt. Allgemeine Limnologie, Max- Planck- Institut fur Limnologie, Postfach 165, D 2320 Plon, FR. G .

Keywords: Keratella cochlearis, morphological variation, cyclomorphosis, Lauterborn cycle, taxonomy

AbstractThe existence of separated forms within the population of Keratella cochlearis (Gosse) from Lake PluBsee

was demonstrated on the basis of a biometric analysis . The morphs cochlearis, hispida and tecta weredefinitely not connected by transitional forms . Micracantha and tecta were not links of a macracantha-mi-cracantha-tecta-series . Hence, the general validity of Lauterborn-cycles is questioned . In this connection, thetaxonomy of this species is also involved, because it is derived from the idea of phenotypic cycles in the senseof Lauterborn .

Introduction

In the limnetic zooplankton Cladocera and Ro-tatoria tend to exhibit substantial morphologicalvariation. The descriptions of these variations andthe discussions of their background have led to avoluminous literature, a considerable part of whichdeals with the rotifer Keratella cochlearis (Gosse) .

As in other species, an important question is,how far is the variability of genetic origin and towhat extent is it caused by the environment (Ker-foot 1980)? In this respect, the papers by Lauter-born (1900, 1903) play an important role in the caseof K. cochlearis . He found the different morphs oc-curring during summer to be descended from auniform winter form by temporal variation andconnected by transitional forms . This conceptstresses the role of environmental factors changingseasonally. Recently, Ruttner-Kolisko(1972, 1974)summarized in a diagram ways in which ecologicalfactors determine the morphological variation inthe species. The current view of the taxonomicranks of the forms of K. cochlearis has also beenderived from the concept of Lauterborn (s . Koste1978).

However, in some cases, results of intensive stu-

Hydrobiologia 101, 247-254 (1983) .© Dr W . Junk Publishers, The Hague . Printed in The Netherlands.

dies were not congruent with this (Ahlstrom 1943 ;Pejler 1957 ; Nauwerck 1978). Hutchinson (1967),reviewing the literature on cyclomorphosis in K.cochlearis, proposed the existence of sibling speciesto explain the morphological variation, assuminggenetic differences . Generally, results from moderngenetic research in planktonic rotifers (King 1972,1977) spotlight the importance of the genetic back-ground in the population dynamics of the animals .However, the discussion on the evaluation of therole of genetic and non-genetic factors determiningthe morphological variation in K. cochlearis is stillopen (Pejler 1980) .

One point at issue is the generality of Lauterborn-cycles . Populations exhibiting discontinuous varia-tion during summer in the same water body areadequate objects for checking whether the formsare connected by transitional lines .

Investigations of summer populations of K.cochlearis in northern German lakes showed that,generally, three morphs co-occurred : K. cochlearis(Gosse), K. cochlearis var . tecta f. typica, and K.cochlearis var . hispida f. typica (Lauterborn) (no-menclature according to Koste 1978), which werewell separated by body length, spine length, andother morphological characteristics such as pres-

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Fig. 1 . Keratella cochlearis, Plul3see 1977 : length of caudal spineagainst length of lorica for all samples (squares : cochlearis,crosses: hispida, rhombs: micracantha, black triangles : recta).

ence of spinules on the lorica . Furthermore, therecta form obviously did not derive from cochleariscochlearis by allometric growth because tecta waslarger than cochlearis (Hofmann 1980) .

In order to verify these results, observations weremade of the seasonal changes in a K . cochlearispopulation from Lake Pluf3see . Lorica length and

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length of the caudal spine of 20 to 60 specimensfrom sample series from three years (1969, 1970,1977) were measured and morphological character-istics were examined in monthly or biweekly inter-vals. In total, 1764 specimens were examined(Hofmann 1981) .

Results

A plot of spine length against lorica length for allspecimens from the year 1977 results in a pattern ofpoint clusters indicating three separated units (Fig .1): (1) a large cluster (squares and crosses) withconsiderable variation in spine length and loricalength, (2) a cluster (rhombs) characterized by veryshort spines, and (3) forms without a caudal spine(black triangles) .

However, if the data from the individual sam-pling dates are considered, it becomes apparent thatthe large cluster consisted of two, well-separatedunits, as seen in Figs . 2, 3 & 4 . With respect to thesetwo forms, in the course of time from spring tosummer, two things happened (Fig. 2 & 3) . Firstly,the specimens of both groups became smaller . Atthe beginning of May, most of the animals of eachgroup were larger than 90 µm and their spines werelonger than 50 µm . Then the point clusters began towander downwards, indicating decreasing spinelenght. In July, most of the specimens were smaller

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Fig. 2 . Keratella cochlearis, Lake Plul3see 1977: length of caudal spine against length of lorica on 4 .4 ., 2 .5 ., and 9 .5 . (symbols as in Fig . 1) .

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Fig. 3 . Keratella cochlearis, Lake Plul3see 1977 : length of caudal spine against length of lorica on 13 .6 ., 27 .6 ., and 13 .7 . (symbols as in Fig .1) .

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Fig . 4. Keratella cochlearis, Lake PluBsee 1977 : length of caudal spine against length of lorica on 7 .11 ., 21 .11 ., and 19 .12 . (symbols as inFig . 1) .

than 80 µm. During autumn, the size of both lorica the animals of the cluster indicated by crosses be-and caudal spine increased again (Fig . 4) . At each of came typical hispida forms with conspicious spin-the sampling dates there were two separate point ules on their lorica . This did not happen in the otherclusters, each showing a decrease and increase in

group .size during the year. In the second place, in summer

SEM-micrographs made evident that in early

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spring the specimens of the hispida group alreadyhad very small pustules . These pustules increased insize from spring to summer and then decreasedagain. In early spring and winter they can hardly beseen with a light microscope .

Referring to Koste (1978), the forms could beidentified as K. cochlearis cochlearis (Gosse) and K.cochlearis var . hispida f. typica (Lauterborn), in thefollowing called cochlearis and hispida, respective-ly .

The seasonal variation in the mean values oflorica length and spine length clearly showed thedecreasing and increasing size during the course ofthe year (Fig . 5 ; hl, hs, cl, cs) . The differences in themean values between hispida and cochlearis werehighly significant . The 95% confidence intervalswere calculated. They were so small that they couldnot be plotted in the scale of the diagram .

In both forms the caudal spine was relativelylonger in larger animals than in smaller (tachyauxe-sis) (Hutchinson 1967) . In cochlearis the relation ofmean lorica length/ mean spine length ranged from1 .24 to 1 .42 in April, May and from October toDecember, and from 1 .52 to 1 .71 from June toSeptember. In hispida the values were generallysmaller, indicating that the caudal spine was rela-tively longer : 1 .12-1 .21 in spring and autumn, and1 .28-1 .33 in summer .

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Fig . 5 . Keratella cochlearis, Lake Plul3see 1977: mean length ofcaudal spine and lorica of the forms cochlearis, hispida, recta,and micracantha against time (hl, hs: lorica, spine of hispida ; cl,cs : lorica, spine of cochlearis ; tl, ts : lorica, spine of recta ; ml, ms :lorica, spine of micracantha) .

The remaining two point clusters in Fig . I cor-respond to the short spined K. cochlearis var . rectaf. micracantha (Lauterborn) (rhombs) and thespineless K. cochlearis var . tecta f. typica (Lauter-born) (black triangles) referring to Koste 1978, inthe following called micracantha and recta, respec-tively .

In 1977, the course of development was as fol-lows (Figs . 2-4) . In winter there were specimens ofthe hispida forms only . In the beginning of May thefirst cochlearis forms were observed . Then bothmorphs underwent temporal variation (decreasingand increasing length of lorica and caudal spine) .The spineless tecta appeared in June, exhibiting alarge gap in spine length to cochlearis . The fourthform, the short spined micracantha, was observedin autumn . It became most abundant in Novemberand December .

The separation of the forms is also evident fromFig. 5 . Cochlearis and hispida exhibited a synchro-nous temporal variation in size . Tecia was interme-diate in size between cochlearis and hispida duringsummer, the differences of the mean values of thethree forms always being statistically significant . Inautumn, the differences between cochlearis and tec-ta were compensated by a rapid increase in loricalength of cochlearis . Additionally, micracantha ap-pearing in November was of the same size range .

The separation of micracantha and cochleariswas obvious. In November, when spine length in

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Fig. 6 . Keratella cochlearis, Lake PluI3see 1969 : mean length ofcaudal spine and lorica of the forms cochlearis and hispidaagainst time (abbreviations as in Fig. 5) .

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Fig. 7 . Keratella cochlearis, Lake Plul3see 1970, 1977 : meanlength of caudal spine against mean length of lorica (numbersindicate months of sampling) .

cochlearis was rapidly increasing, the spine lengthof micracantha was even lower than that of coch-learis in July and August. Furthermore, the relationof lorica length/ spine length was quite different inthe two morphs (Fig. 5) .

Concerning the occurrence of the forms underdiscussion, considerable changes occurred from ye-ar to year . In 1969 and 1970 specimens of the formstecta and micracantha were not found at all . Inother respects, the variation in K . cochlearis fol-lowed the same pattern as in 1977 (Figs . 5 & 6) :throughout the year there were two groups withinthe population, always well separated and identicalwith the forms cochlearis and hispida found in1977 .Figure 7 shows the cyclomorphotic loops (Ker-

foot 1980) of the two forms indicating two separat-ed phenotypic cycles . There is some overlap be-tween the loops because the summer specimens ofhispida were in the range of the winter specimens ofcochlearis .

The dimensions of morphological variation with-in the different forms may change from year to year .This becomes evident when the data from 1970 and1977 are compared (Fig. 7) . In 1977 spine lengthvaried much more in cochlearis as well as in hispidathan in 1970, because in both forms the caudal spinebecame significantly shorter in summer . Generally,

there was no perfect correlation between the varia-bles (length of caudal spine versus length of lorica) .This was due to the fact that the spine was relativelylonger in autumn than in spring .

In summer 1977 the variables were more closelycorrelated : the points formed a straight line forboth forms. However, in October the lines of de-creasing and increasing spine length diverged asthey did in 1970 (Fig . 7) .

The 1977 data did not produce a closed loop inthe case of cochlearis because absolute spine lengthwas much longer in autumn than in spring (Fig . 5)Probably, additional data from the winter of 1978would have closed the loop .

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Fig . 8 . Keratella cochlearis: Scheme of morphological variationaccording to a Lauterborn cycle (upper panel) and to the situa-tion in Lake Plul3see 1977 (lower panel) .

252

Discussion

The results show the presence of distinct morpho-logical forms in the population of Keratella coch-learis from Lake PluBsee . These morphs were se-parated throughout the year even though each ofthem exhibited temporal variation . This variationdid not lead to transitional series between the formsunder discussion (Fig. 8) .

Specifically, hispida and cochlearis did not de-rive from a uniform winter form in common, nordid tecta and micracantha derive from cochlearis .The temporal variation in cochlearis led to smalleranimals with shorter spines in summer, but no evi-dence was found for a transition to tecta and micra-cantha. Tecta was larger than cochlearis and hencecould not have derived from cochlearis by allomet-ric growth of the caudal spine . There was always adistinct gap in spine length between the forms .Furthermore, tecta and micracantha occurred inthe lake when body size and spine length of cochlea-ris were increasing . Finally, the relation of loricalength/ spine length clearly differed in cochlearisand micracantha .

Possibly, there was a connection between micra-cantha and tecta, because micracantha was onlyfound in those years when recta occurred duringsummer. It only appeared in autumn at low tem-peratures and might therefore have derived fromrecta by allometric growth of the spine . However,there were no true transitional forms with extreme-ly short spines, as reported for instance by Lauter-born (1900) and Pejler (1962) . Furthermore, therewas no significant difference in body size betweenrecta and micracantha .

Pejler (1980), discussing similar cases of discon-tinuous variation within a single lake, mentionedhat the different forms might have been developeddue to different ecological conditions as, for in-stance, in the epilimnion and the hypolimnion .However, in Lake PluBsee this was obviously notthe case because during the summer of 1977, whenhispida and cochlearis co-occurred and recta ap-peared additionally, the epilimnion was only 4 mdeep and there was no oxygen in the hypolimnion .Hence, there was no space for vertical separation ofthe forms. Nevertheless, it is desirable to examinethe vertical distribution of the morphs . This was notpossible on the basis of the material presented here .

Lake Plul3see is an isolated water body, so immi-gration of animals from surrounding lakes is anunlikely explanation for the polymorphism ob-served. This point has been considered by Pejler(1980) in the case of populations from Swedishlakes .

The temporal variation within the assemblages ofthe distinct morphs, e .g. increase and decreasee ofsize, is related to environmental conditions, espe-cially to food and temperature (Buchner et al . 1957 ;Pejler 1962 ; Hillbricht-Ilkowska 1972; Lindstrom& Pejler 1975) .

However, the development of the differentmorphs cannot be related to ecological factors, be-cause they were exposed to almost the same envir-onment. The splitting up of Keratella cochlearisinto separated forms can only be explained as ofgenetic origin. The application of the iso-enzymemethod (King 1977) may give more information inthis respect .

The results presented are in accordance with thefindings of other authors . For instance, Ahlstrom(1943) questioned transitional lines from cochlea-ris to hispida . Carlin (1943) suggested the possibili-ty of genetic isolation between the tecta- and hispi-da-Reihe. Pejler(1962) found K. cochlearis popula-tions in some cases apparently divided "into threeseparate forms" . Hillbricht-Ilkowska (1972) gavean example of co-occurrence of cochlearis and tec-ta . Her data showed the influence of food andtemperature on the size of these animals but also theseparation of cochlearis and tecta: Tecta cannot beexplained as a cochlearis-form with total spine re-duction due to allometric growth of lorica andspine, because tecta specimens from 20 m waterdepth were larger than cochlearis from the epilim-nion . Nauwerck (1978) doubted that tecta fromLake Ontario could be considered as the "end of amacracantha-micracantha strain" . Furthermore, hefound the K. cochlearis population to be dividedinto different size classes during winter, too . Baker(1979) demonstrated that Keratella cochlearis andK. earlinae Ahlstrom coexisting in Hasting Lake(Canada) are not ecophenotypes but distinct spe-cies .Thus, many empiral studies give evidence that

separated "sub-populations" of K. cochlearis existand that Lauterborn-cycles do not generally occur .Hutchinson (1967) suggested the existence of si-bling species in the case of the hispida and recta

forms. Recently, Pejler (1980) indicated the occur-rence of "camouflaged sibling species" as a possibleexplanation for discontinuous variation in K. coch-learis . The different morphs from Lake Plul3seeindeed behaved like distinct species rather thanmembers of the same populations .

This view is supported by the observation thatthe forms cochlearis, hispida, and tecta, co-occur-ring in many northern German lakes, are morpho-logically distinct in the same habitat, and are hom-ogeneous groups if specimens of a distinct morphfrom different lakes are compared (Hofmann1980) . The impression is of separated, defined, andhomogeneous units, at least in the area under dis-cussion .

This point inevitably leads to the question of thetaxonomic rank of these forms . Unfortunately, re-cent revisions of rotifer taxonomy have shown noconsensus on the question in the case of K. cochlea-ris: Kutikowa (1970) considered them as subspeciesof K. cochlearis (for example : K. cochlearis hispida(Lauterborn)). Ruttner-Kolisko (1974) consideredthem as forms (for example : K. cochlearis f. hispi-da), and Koste (1978) called tecta and hispida varie-ties, micracantha a form of the variety tecta, andthe form mentioned above as cochlearis as a sub-species (K. cochlearis cochlearis (Gosse)) assumingtecta and hispida to be genetically isolated andmicracantha to be a morph of a polymorphic popu-lation .Without evidence of the genetic isolation, it

seems most convenient to call them forms (as Rutt-ner-Kolisko (1972, 1974) did), as the term varietyshould be avoided and the term subspecies is inap-propriate for sympatric populations . The termtecta-Reihe, presuming transitional series betweenmacracantha - cochlearis - micracantha - recta bytemporal variation, should be abolished . Suchtransitional lines can only be established on thebasis of direct observations . More data from differ-ent biotopes and different regions are needed in thisrespect .

The true taxonomic ranks of the forms remainambiguous due to the almost exclusive parthe-nogenetic reproduction in many populations(Pejler 1957). An examination of the iso-enzymeswill probably not settle the problem . If K. cochlea-ris turns out to be heterogeneous for iso-enzymes insome cases, this will not automatically lead to theassumption of distinct species because natural pop-

253

ulations may be polymorphic in this respect (King1977) .The results presented here again show the advan-

tage of the nondimensional species concept (Mayr1967) which leads to easy separation of sympatricmorphs . However, a form like tecta cannot be desc-ribed as a species based on results from a singlelake, i .e. on only one population . A species is a unitconsisting of many populations which should all berepresented in the description .

Acknowledgements

I wish to thank Dr . H.-J. Krambeck, who madethe computer calculations of the data (mean values,confidence intervals) and the computer diagrams,and Richard Bohrer for his help in preparing theEnglish text .

References

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Baker, R. L ., 1979 . Specific status of Keratella cochlearis(Gosse) and K . earlinae Ahlstrom (Rotifera : Brachionidae) :morphological and ecological considerations . Can . J . Zool .57 :1719-1722 .

Buchner, H ., Mulzer, F . & Rauh, F ., 1957 . Untersuchungenfiber die Variabilitat der Radertiere . I .) Problemstellung andvorlaufige Mitteilung"uber die Ergebnisse . Biol . Zbl. 76 :289-315 .

Carlin, B., 1943 . Die Planktonrotatorien des Motalastrom .Medd. Lunds Univ. Limnol . Inst . 5 : 1-256 .

Hillbricht-Ilkowska, A ., 1972 . Morphological variation of Ke-ratella cochlearis (Gosse) Rotatoria) in several Masurianlakes of different trophic level . Pol . Arch . Hydrobiol . 19 :253-264 .

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Koste, W ., 1978 . Rotatoria . Borntraeger, Berlin, 2 Vols, 637 pp .,234 plates .

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Received 18 January 1982 ; in revised form 25 August 1982 ;accepted 25 August 1982 .