Morphological differentiation and geographical distribution of the Lemna gibba-lemna minor group

Aquatic Botany, 1 (1975) 345--363 © Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

MORPHOLOGICAL DIFFERENTIATION AND GEOGRAPHICAL DISTRIBUTION OF THE LEMNA GIBBA--LEMNA MINOR GROUP

ELIAS LANDOLT

Geobotanical Institute (The R~bel Foundation), Swiss Federal Institute o f Technology, ZUrich (Switzerland) (Received May 9th, 1975)

ABSTRACT Landolt, E., 1975. Morphological differentiation and geographical distribution of the Lemna gibba--Lemna minor group. Aquat. Bot., 1: 345--363. A 100 strains of Lemna gibba L. s. 1. and 350 straius of L. minor L. s. 1. have been morphologically investigated from a collection of living strains. The following characters have been considered (Table I): shape and size of root-cap, shape and size of fronds, structure o f the upper surface, gibbosity, innervation, pigmentation and turion formation. A new feature, useful in differentiation of L. gibba s. 1. and L. minor s. 1. is given in the number and disposition of the nerves (Fig. 2). The systematic position of L. disperma Hegelmaier and L. parodiana Giardelli could not be clarified because there were not enough flowering plants. Both taxa seem to occur within the ecological and geographical limits o f L. gibba s. str. L. minor s. 1. can be subdivided into three taxa according to morphological, geographical and ecological features: L. minor L. s. str., L. obscura (Austin) Daubs and L. turionifera spec. nov. L. turionifera differs from L. minor mainly by the formation of turions and the pigmentation of the lower surface of fronds. L. obscura is able to produce gibbous fronds; further, the prominent papilla at the apex and the pigmentation of the lower surface are typical. Measurements performed in aquatic habitats of various Lemna species in North America show that L. gibba colonizes waters that show the highest concentration of calcium, magnesium, sodium, nitrogen and phosphorus. The lowest concentrations have been found in waters with L. minor s. str. (Table II). The geographical distribution of L. gibba s. 1. is distinctly limited by climatic boundaries towards too cold, too warm and t o o wet regions. The boundary against too cold areas is fairly coincident with the January isotherm of about - 1 ° C. The limit against warmer areas is given by the 18 ° C isotherm of the three coolest months. Further limits are given by precipitations of at the utmost 90 m m / y e a r or by the absence of a dry period during the growing season. The regions situated outside the 10 ° C isotherm for the three warmest months are t o o cold for L. minor s. l.; on the other hand, areas where the isotherm for the three coolest months is higher than 15 ° C are apparently too warm. L. turionifera occupies more continental regions of North America and eastern Asia, characterized by low amount of precipitations and low minimal temperatures. L. minor s. str. grows in rather a moist climate, being rare or absent in more arid regions. L. obscura is confined to the south-eastern United States that have mild winters and h o t humid summers. The distributional limits have to be explained partly by the competition between various species of Lemnaceae.

346 INTRODUCTION

The species delimitation within the family of the Lemnaceae and the distribution of the various species are still not clear on many points in spite of the numerous publications on Lemnaceae, most of them in the physiological domain. This may be due to the following factors: (1) All vegetative and reproductive organs of the Lemnaceae are much reduced, so the morphological differentiation within the family is confined to few, often hardly recognizable, features. (2) Most of the few diagnostic characters are strongly liable to modification by external factors (temperature, light intensity, quality and concentration of nutrients in the water, etc.). Strongly modifiable features are for instance: size and shape of fronds, gibbosity, length of roots, size of air spaces, colour and pigmentation of fronds. Thus, most of the characteristics of closely related species overlap, and a comparison between the taxa is often only possible when they are cultivated under equal conditions. (3) Since vegetative propagation dominates within most species, plants occurring in a given region often represent clones. For this reason, it is difficult to determine the total range of variation of a particular species. Morphological features which are different in two clones tend to be easily overestimated, whereas such differences often correspond to inter-individual variability of other flowering plants. (4) Hybrids within the Lemnaceae have only exceptionally been reported (Kandeler, 1975). On the other hand, if hybrids occur, they might become stabilized through vegetative reproduction and contribute in this way to some intergradation between certain species. Within the family of the Lemnaceae, delimitation of the group of Lemna gibba--L, minor is particularly difficult. Hegelmaier co-ordinated L. gibba L. and L. minor L. in his monograph of 1868 to two different subgenera, since L. gibba has more than one ovule in contrast with all the other species of Lemna. However, the diagnostic value of this character is not satisfactory because the very rare flowering of the species renders a quick identification almost impossible. The diagnostic importance of the number of ovules was further reduced by the discovery of two taxa that take an intermediate position in this respect: Hegelmaier himself described in 1871 L. disperma, and Giardelli (1937) recorded a new species under the name L. parodiana. Both these taxa have fruits with one to two seeds. Den Hartog and Van der Plas (1970) were apparently right in placing L. gibba and L. minor within the same subgenus of Lemna. The present paper reports some observations that were carried out recently on living material, both in culture and under natural conditions. I shall try to give a general view of the morphological, ecological and geographical differentiation within the group.

347

MATERIAL

The establishment of our collection of live plants of the Lemnaceae was begun in 1953. Originally it consisted of 80 strains, mostly from California, which were physiologically investigated (Landolt, 1957). Since 1966 the collection has been systematically enlarged in connection with the cytological studies of Dr Urbanska-Worytkiewicz. We received live plants of the Lemnaceae from all over the world• I am deeply impressed by the generous co-operation from hundreds of colleagues and wish to express here m y sincere thanks for their inestimable help. A detailed list of individual co-operators will follow in a further publication. We have received in this way about 1,300 strains, 800 of which are still being kept in culture. It is planned to reduce this n u m b e r to half, because maintenance of the collection requires an enormous a m o u n t of work and time. Fig. 1 shows the origin of the various strains of our collection within the total area of the Lemnaceae. Some regions are richly represented, others remain to be investigated in detail. For L e m n a gibba and L. minor, which avoid warm tropical regions, the following gaps should be mentioned: 1, Central and northern Asia; 2, northern Canada and Alaska; 3, western and eastern Australia; 4, High mountains and southern parts of South America. Approximately 100 strains of L. gibba s. 1. and 350 strains of L. minor s. 1. have been investigated.

..

_ _

• O r i g i n o f the i n v e s t i g a t e d Lemnaceae - - - - - l i m i t o f general area o f the Lemnaceae

Fig. 1. Origin of the live specimens of the Lemnaceae investigated.

348

MORPHOLOGICAL OBSERVATIONS

Plants of the L e m n a gibba--L, minor group are morphologically the least reduced within the genus Lemna. Characteristic features of the group compared with the other species of the genus are the following. Fronds floating on the surface of the water, sometimes pigmented (reddish) on the upper or lower surfaces, gibbous or flat, with three to five nerves. R o o t s up to 15 cm long; r o o t sheath n o t winged; root~cap in living material obtuse. Seeds 1--6 in number. The following features are n o t k n o w n in any other species of Lemna: pigmented lower surface of the frond, gibbous fronds, more than three nerves, roots longer than 3 cm, more than one seed and obtuse root-caps (except occasionally in L. valdiviana s. 1.). The following characters were considered during the morphological study on the L e m n a gibba--L, minor group: shape and size of the frond, structure of the upper surface of the frond, gibbosity, innervation and pigmentation of the frond, shape and size of the r o o t ~ a p , turion formation. The numbers of ovules and seeds were not investigated in detail because there was n o t enough flowering matei-ial available. Morphological treatment o f the group requires a detailed study on flowers and fruits. Shape and size o f frond. -- Shape as well as size of the frond are strongly influenced by external conditions and therefore are of no great diagnostic value. A s y m m e t r y can be marked to different extents according to conditions, even within the same clone. The length/width ratio of m a n y strains of L. minor is, under certain conditions, greater than that of L. gibba, but this characteristic is not very useful because o f its great variability. Fronds with a ratio of more than 3/2 belong mostly to typical L. minor. Size of frond is also liable to modification. Moreover, there exist distinct genetic differences between various strains from the same region. Thus, small and large fronds can be found within L. gibba originating from the same place (e.g. California, Argentine). On the other hand, there are regions where L. minor s. 1. shows a smaller or bigger average size of the fronds. Plants of L. minor collected in New Zealand or in Australia are on the average smaller than those from Europe. Smaller plants also occur in North America, especially in the western and southern parts. Structure o f the upper surface o f the frond. -- The structure of the upper surface is also often influenced by external factors.More or less distinct papillae or papules can be observed in all strains. Particularly n o t e w o r t h y is a papilla at the node as well as that at the apex. When the fronds thicken, these papillae disappear, totally or partially. They are usually more developed in small than in larger fronds. The papilla at the apex is especially well marked in plants of L. gibba s. 1. from Australia. The most prominent papilla at the apex was found in plants of L e m n a minor s. 1. from the south-east of North

349 America; it was as big as t h a t occurring within L. perpusilla Torrey s. 1. L . m i n o r often shows papules along the m e d i u m nerve; t h e y are distinctly marked on plants coming from middle and western North America and on those from eastern Asia. Gibbosity o f fronds. -- There is a possibility of considerable thickening of the fronds by enlargement of the air spaces downwards for all strains of L. gibba s. 1.; however, this thickening occurs only in certain conditions that are not exactly the same for all strains. The problem of gibbosity has recently been investigated by Pieterse et al. {1970), De Lange (1975) and Pieterse (1975). However, strains with genetically fixed flat fronds are placed by the present author within L. minor s. 1. The fronds of L. minor s. l., except for those from the south-east of the United States, m a y become a little thicker under certain conditions, but never become gibbous. Innervation. -- L. gibba s. 1. characteristically shows four to five nerves when grown in favourable conditions; this is usually true of the small forms, too. L. minor has less frequently four or five nerves. Most strains from the southern Hemisphere, as well as numerous strains from North America (especially from the south-east and west), form only three nerves under the cultural conditions used. Strains from Europe, south-east Asia and from m a n y places of North America often form four or five nerves under favourable conditions. It should be added that in L. gibba all nerves are branched from the base, whereas L. minor has the outermost nerves connected with those on the innerside at some distance from the base (Fig. 2). Pigmentation. -- All taxa of the group are able to form anthocyanins on the upper surface of the frond given certain conditions (cold temperatures, deficiency of nutrients connected with a high light intensity). This pigmentation is diffusely distributed over the whole surface of the frond. Moreover, a characteristic pattern of pigmentation occurring near the apex was sometimes observed in L. gibba. However, it cannot be decided whether this detail is a general character for all strains of L. gibba s. 1. The lower surface of the fronds of L. gibba is sometimes red. This colouring usually begins at the edge of the surface, in the surrounding cells of the air spaces, or on the nerves. In L. minor from Europe, Africa, western Asia, Australia and New Zealand, as well as from some parts of North America, no red colour of the lower surface of the frond was observed, whereas it occurred in the material from the southeast and the west of the States, from Hawaii and eastern Asia. The plants from the south-east of the States were nearly always deeply coloured. The colouring of L. minor s. 1. begins at the base of the root. Shape and size o f the root-cap. -- Hegelmaier (1868, 1896) attached great importance to the shape of the r o o t ~ a p as a diagnostic character of L. gibba and L. minor. The latter species was said to have obtuse tips of root-caps, the former being characterized by acute tips. Nevertheless, Hegelmaier indicated

P

~0 0

0

J

f

j

..,~°

351

some exceptions. In our cultures, all strains of L. gibba and L. minor show the same, more or less obtuse, tip of the root-cap; sometimes a protruding cell m a y suggest a pointed tip. This characteristic feature was n o t altered in most of our herbarium samples. On the other hand, the foot,cap of L. gibba detaches itself somewhat from the r o o t and becomes pointed in the drying process when the roots dry o u t before they are pressed (Fig. 3). The length of the root-cap varies within the same strain on different fronds. On the average, it is longer within L. gibba (0.6--1.8 mm) than within L. minor (0.4--1.1 mm).

mm

0,2 0,4

I° 0,6 0,8

Lemna qibba s . l .

Lemna minor s . l ,

Fig. 3. F o r m of root-caps o f Lemna gibba s. I. and L. minor s. 1. f r o m fresh material (left) and f r o m dry specimens (right).

Turion formation. -- As in Spirodela polyrhiza (L.) Schleid., some strains of L. minor form pigmented, more or less orbicular and rootless turions that sink to the b o t t o m of the water. Under unfavourable conditions and sufficient light intensity, L. gibba and most strains of L. minor develop small fronds, rich in starch, that deviate from the c o m m o n fronds only by their size; they seldom sink to the b o t t o m . Turion-forming strains originate from the western and the northern parts of the United States, from Canada and from eastern Asia. N u m b e r o f ovules. -- According to Hegelmaier, the number of ovules is a key character to distinguish between L. gibba and L. minor; L. minor is said to have only a single ovule, L. gibba t w o to six ovules. Preliminary studies on flowering plants show that all the fronds of L. minor s. 1. investigated, indeed have single ovules. On the other hand, we found in L. gibba s. 1. one to four

++ Frequently occurring and pronounced + Infrequently occurring and not pronounced (+)Only rarely occurring and not pronounced - Not occurring

+

--

L. minor

+

++

--

(+) (+) (+)

Papules along the medium nerve

L. turionifera

+

+

Papilla at apex

+

++

Gibbosity

L. obscura

L. disperma

L. parodiana

L. gibba

Taxon

Morphological characters of the Lemna gibba--L, minor group

TABLE I

I

_ [-~

-

-

-

Turions

[~

-

+

+

Lower surface pigmented

-

(+)

++

+

f~]

1--3

1--3

1--6

Pigment spots Number of near the apex ovulesa of upper surface

* When four to five nerves occur, all nerves remain branched from the base ** When four to five nerves occur, the outermost nerves are connected with the innerside nerves at some distance from the base a Only preliminary counts, partly completed from indications of Hegelmaier (1896) and Giardelli (1937)

(+)** (+)**

(+)*

+ *["

++*

Four to five nerves

CO t~

353 ovules; it is interesting to note that only one ovule was found in very gibbous and large fronds from South Africa. It seems that the number of ovules is n o t always a reliable feature: plants with more than one ovule belong to L. gibba s. 1., b u t plants with a single ovule might belong either to L. gibba s. 1. or to L. minor s. 1. Only limited material has been investigated in the present work; therefore, it cannot be decided whether plants of L. gibba are always able to form more than one ovule if the conditions are favourable, or if there are genetically fixed clones with only a single ovule. More detailed studies in this respect are being continued. The morphological differences within the L. gibba--L, minor group are presented in a summarized form in Table I. Supplementary indications are briefly given below. Lemna gibba L. s. I. Fronds very often gibbous, with a length/width ratio of I to 3/2, never with distinct papules on the medium nerve (except at the node and the apex}, sometimes with characteristic pigment spots on the upper surface near the apex, sometimes pigmented on the lower surface (the colouring usually begins at the edge of the surface, in the surrounding cells of the air spaces or on the nerves), with three or more often four to five nerves (nerves remaining separate from the base). Plants n o t forming characteristic turions, similar to those of

Spirodela polyrhiza. Whether and h o w far L. gibba can be subdivided, is a matter for further investigation. L. parodiana described by Giardelli (1937} is smaller than a typical L. gibba, shows a distinct papilla at the apex, has only one to t w o seeds and characteristic pigment spots near the apex of the upper surface. We have in our collection only a few strains that correspond to this description, one from Argentina and four, n o t quite identical, from California. The strain from Argentina was collected in the same station as a strain of a typical L. gibba. Both strains preserved their characteristic features in culture (Figs 4A, 4B}. The strains with small fronds originating from California are situated geographicaily and ecologically within the distribution area of L. gibba. In addition, the prominent papilla at the apex m a y occur in small fronds of L. gibba from other regions, and the pigmentation pattern described as specific for L. parodiana was observed in some strains with larger fronds. We cannot therefore decide whether L. parodiana represents a separate taxon or should rather be considered to represent a clone showing extreme morphological features yet remaining within the variation range of L. gibba. Likewise unclear is the taxonomic rank of L. disperma, described b y Hegelmaier (1871) from western Australia and reported b y Giardelli (1941) from Argentina. We have not seen any material from Argentina. Strains from Australia are assigned in the present article to L. gibba s. 1. They are characterized by a more prominent papilla at the apex (Figs 4D, 4E). The fronds of some strains are as large and gibbous as the largest of a typical L. gibba (Fig. 4D) and also have five nerves. The

354

fronds of most other strains are much smaller, rarely become gibbous and were never observed to have the characteristic pigmentation of some strains of a typical L. gibba. Thus, it is difficult to distinguish them from L. minor. Until recently we assigned them to L. minor. Only an occasional occurrence of more than three nerves, arranged as those in typical L. gibba, as well as a slight

o

2

4

6~

Fig. 4. Live fronds of the Lemna gibba--L, minor group grown under the same conditions (1/10 Hutner's solution, 16 h light o f 30,000 lux, 28 ° C day temperature, 18 ° C night temperature). A: L. gibba s. str. (No. 7922, large fronds) and L. parodiana (No. 7922a, small fronds) from the same place in Argentine. B: the same as A, but the lower surface of the fronds. C: L. gibba s. str. (No. 7007) from northern Italy -- fiat fronds, partly flowering. D: L. gibba (No. 7816a) from South Australia. E: L. disperma (No. 7276) from Victoria, Australia. F: L. minor s. str. (No. 6578) from Switzerland. G: L. turionifera (No. 6573) from Montana, U.S.A. - the small fronds are turions. H: the same as G, but the lower surface of the fronds; turions smaller and without roots. I: L. obscura (No. 7856) from Louisiana, U.S.A.

355 gibbosity of the fronds when grown in culture medium with EDDHA, point to a close relationship to L. gibba. We have n o t y e t investigated in detail the flower structure. The definitive taxonomic status of L. disperma requires further study. Lemna minor L. s. str. (Fig. 4F) Fronds never becoming inflated, sometimes with a length/width ratio more than 3/2, rarely with distinct papules on the medium nerve (except at the node and at the apex), w i t h o u t characteristic pigment spots on the upper surface, w i t h o u t pigment on the lower surface, with three to five nerves (when with four or five nerves, the o u t e r m o s t connected with the inner nerves at some distance from the base (Fig. 2). Plants n o t forming characteristic turions, similar to those of Spirodela polyrhiza. Plants from New Zealand and Australia are, on the average, smaller than those from Europe. Lemna turionifera sp. nov. (Figs 4G, 4H) Plantae Lemnae minoris affinis. Frons elliptico-orbicularis, 1--3 mm longa, 1--3 mm lata, 3(--5) nervis, supra nerva media cum 3--7 papillis, infra saepe pigmentata, (imprimis circum basim radicis). Plantae conditionibus iniquis turiones parvas, rotundatas pigmentatasque sine radice faciens. Type specimen: U.S.A., Montana, Lincoln Co., 20 km west of Davensport. Leg. Wm. M. Hiesey, June 19th, 1953. Herb. ZT (Ziirich, Switzerland). Live collection No. 6573. Fronds never becoming inflated, with a length/width ratio of I to 3/2, very often with three to seven distinct papules on the medium nerve, w i t h o u t characteristic pigment spots on the upper surface, often pigmented on the lower surface (the colouring beginning at the base of the root), mostly with three nerves (when with four or five nerves, the o u t e r m o s t connected with the inner nerves at some distance from the base (Fig. 2). Plants forming characteristic turions, similar to those of Spirodela polyrhiza. Fronds with more than three nerves were only observed in material from eastern Asia and Hawaii. Most of the plants named L. turionifera by the present author, were considered by Daubs (1965) to be flat forms of L. gibba. However, they have, in m y opinion, no typical characters of L. gibba apart from the pigmentation on the lower surface of the frond. It should be noted that strain 6573 showed no sign of gibbosity after being cultured on E D D H A (De Lange and Pieterse, 1973). Lemna obscura (Austin) Daubs (Figs. 4D Fronds sometimes gibbous, with a length/width ratio of 1 to 3/2, with a

356

prominent papilla at the apex (similar to that of L. paucicostata Hegelm.), sometimes with three to five distinct papules on the medium nerve, without characteristic pigment spots on the upper surface, very often deeply red pigmented on the lower surface (the colouring beginning at the base of the root), mostly with three nerves (when exceptionally with four or five nerves, the outermost connected with the inner nerves at some distance from the base (Fig. 2). Plants not forming characteristic turions similar to those of Spirodela polyrhiza. L. minor vat. obscura Austin has been described in Gray (1867). I have checked the type material from New Durham Meadows in New Jersey (Herb. MO). The plants show the characteristic prominent papilla at the apex, big air spaces and a pigmented lower surface. The locality in New Jersey is rather isolated. It seems that this species is occasionally introduced to the Northern States by birds but probably cannot endure cold winters there. The delimitation of L. obscura in the present article is not identical with that of Daubs (1965) and McClure and Alston (1966). In my opinion L. obscura does not occur in California and is rare in the Northern States; most plants from these regions should rather be assigned to L. turionifera. ECOLOGICAL INVESTIGATIONS Numerous ecological investigations have previously been carried out in the Lemnaceae: e.g. Hicks (1932), on pH range in Ohio; Luther (1951), on salt concentration in Finland; Landolt (1957), on pH range and conductivity, in California; Harrison and Beal (1964), on pH range, chloride content and organic content, in North Carolina; De Lange and Segal (1968), as well as De Lange (1972), on conductivity and various nutrient contents in The Netherlands. Since most of these studies were dealing with no more than one species from the Lemna gibba--L, minor group, we only refer to the investigations performed on two or more species. According to my observations (Landolt, 1957), the variation in range of pH within the aquatic habitats of the Lemnaceae was high: for L. minor (= L. minor II) 5.0--7.5, for L. turionifera (= L. minor I) 3.5--8.2, for L. gibba 5.5--8.0. No great differences could be traced between the species. The waters in which the three species were found 'differed from each other in their average salt concentration. It corresponded for L. gibba to a 0.012 mol/1 solution of KC1, for L. turionifera to 0.010 mol/1 and for L. minor to 0.003 mol/1. According to De Lange and Segal (1968), the conductivity of waters with L. gibba fluctuated between 20 and 6,600 x X 10 -6 (18°C), and with L..minor between 10 and 660 x × 10 -6 (18°C). De Lange (1972) reports an even greater range of variation. In waters with gibbous L. gibba, the conductivity wasmostly over 650 x × 10 -6 (25°C), with L. minor mostly below 600 x × 10 -6 (25°C). The so~called "fiat form" of L.ogibba was mostly found in waters with intermediate values of conductivity. The average content of PO4 phosphorus for gibbous L, gibba was over 0.3 mg/1, that on flat L, gibba around 0.1 mg/l whereas the values established forL. minor approached 0.05 rag/1.

pH

8.2 (7.4--9.8)

7.3 (6.8--7.7)

7.7 (7.1--9.8)

7.2 (6.6--7.9)

Samples

15

9

11

11

Taxon

L. gibba

L. minor

L. turionifera

L. obscura

510 (120--2,900)

470 (185--1,300)

320 (70--700)

930 (200--2,600)

Conductivity

22 (4.8--68)

22 (4.0--73)

13 (3.0--32)

40 (6.5--115)

Ca

K

15 (3.3--18)

12 (2.2--53)

32 16 (3.6--100) (5.3--35)

19 (3.9--95)

23 (2.5--85)

66 15 (7.5--145} (3.4--30)

Mg

110 (9--800)

80 (17--225)

40 (10--115)

250 (28--850)

Na

1.4 (0.2--11.2)

1.0 (0.2--2.9)

1.4 (0.4--3.0)

2.1 (0.2--10.6)

N (as NO 3 and" NH4 )

0.18 (0.01--(" 50)

0.08 (0.00-0.35)

0.05 (0.01--0.12)

1.24 (0.02--9.9)

P (as PO, )

Some chemical properties of the water samples from different locations of Lemnaceae in North America. Ions in rag/l; mean values o f the different samples, total variation in parentheses

TABLE II

CO e~

358 During a trip across North America, made in August--September 1973 together with Dr Urbanska-Worytkiewicz, we collected water samples from places inhabited by Lemnaceae, especially in Colorado, Texas, Louisiana and California. We also made various measurements. Our preliminary results are presented in Table II; they will be published in detail later. The following points must be kept in mind for the interpretation of the results: (1) The number of samples investigated was relatively small for each species (9--15); the results can thus only serve as indications. (2) In California, the highest values for pH and salt concentration in the waters were measured in late summer and in early autumn (Landolt, 1957); from our recent measurements, it seems that we obtained the highest values of t h e yearly variation for both factors. It cannot be decided whether this is also valid for the nitrogen and phosphorus contents. The contents in calcium, magnesium, sodium, phosphorus and nitrogen were highest in waters with L. gibba; the same could be said a b o u t pH and conductivity. Only the average potassium c o n t e n t was more or less equal in all waters. Waters in which L. minor s. str. occurs, showed the opposite extreme. L. obscura and L. turionifera grow in waters with a medium c o n t e n t of calcium and sodium. L. obscura has a meditun position as to magnesium and phosphorous contents, as L. turionifera has for pH. The average conductivity and phosphorous c o n t e n t of waters with L. gibba and those with L. minor are of similar orders of magnitude in U.S.A. as in The Netherlands (cf. De Lange, 1972). L. gibba apparently tolerates higher concentrations of nutrients than L. minor, or at least remains more competitive than the latter species. On the other hand, L. minor grows more rapidly in dilute solution (1/100 Hutner's solution) than L. gibba and L. turionifera, whereas all three species propagate with a similar speed in 1/3 Hutner's solution, in temperatures between 20 and 30 ° C. According to the recent observations of WoTek (1974), L. gibba is more competitive than L. minor, when cultures are provided with a good nutrient supply. We can thus presume that L. gibba represses L. minor under favourable nutrient conditions, whereas L. minor develops better in waters p o o r in nutrients. GEOGRAPHICAL DISTRIBUTION The geographical distribution was worked o u t on the basis of our collection of live plants of the Lemnaceae. Additional indications were taken from Hegelmaier's publications (1868, 1896). Regional floristic works were consulted for regions where a confusion with other species is n o t likely to occur. Thus, the northern limit in Eurasia and North America established for L. minor s. 1. was completed with indications found in the literature; the same was done to trace the northern and eastern limits of L. gibba s. 1. in Europe as well as the southern limit of this group in South America. The distributions of L. gibba s. 1. and of L. minor s. 1. are generally similar

359

but n o t at all congruent. Both taxa avoid warm tropical regions; the southern limits in North Africa, Western Asia and Middle America therefore take a similar course; this is also true of the northern limits in South Africa and Australia. In the following sections I shall try to set the geographical limits of the particular species in c o n f o r m i t y with the climatic boundaries. The climatic data were taken from Walter and Lieth (1968). The climatic boundaries worked out for both taxa are n o t absolute, and isolated locations may occur outside the postulated areas. Lemna gibba s. l. (Fig. 5) The occurrence of L. gibba is limited with respect to warm regions by the 18 ° C isotherm of the three coolest months; the limit towards cool regions corresponds roughly to the - 1 ° C January isotherm. Spohr (1926) indicated that the - 5 ° C January isotherm was an absolute limit in Russia. Locations in regions with mean January temperatures between - 1 ° C and - 5 ° C are extremely scarce. In tropical mountains, L. gibba occurs only up to elevations where night temperatures are n o t considerably under 0 ° C. On the lake of Titicaca in Peru, L. gibba reaches, together with L. valdiviana, the highest location known for the Lemnaceae i.e. 3,800 m above see level. As a rule, L. gibba s. I. occurs only in regions with a marked drought season during the vegetation period or with an average yearly precipitation level of less than 90 mm. It is evident t h a t L. gibba s. 1. t o d a y colonizes nearly all adequate places t h r o u g h o u t the world. The absence of L. gibba from the south-eastern,

Fig. 5. Distribution of L e m n a g i b b a s. 1.

360 eastern and north-western states o f the U.S.A. is due to the high precipitation levels; the absence of this taxon in the middle and northern parts o f North America, in northern Europe as well as in central and northern Asia is caused b y the low winter temperatures. The location on St. Thomas Island (the Antilles), reported b y Hegelmaier (1868), is isolated and cannot be climatically explained. It might be that there are locally cooler waters, or the location is erroneous as a result o f a confusion of labels. Lemna minor s. I. (Fig. 6) Distribution of L. m i n o r s. I. in warm regions is limited b y the 15 ° C isotherm of the three coolest months. On the other hand, this species does n o t

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.......t ~actually

known area

turlonifera)

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.... ar~as cll~tici!ly suitable yet with no records

////plants forming turlons ~ p l a n t s (L.

°

--

(L.

with pigmented lower surface turionifera,

L. obscura)

plants wlth gibbous fronds (L.

ObScura)

Fig. 6. Distribution of L e m n a m i n o r s. I.

occur in regions with t o o cool summers. The limits coincide approximately with the 10 ° C isotherm of the three summer months. In arid regions where L. gibba occurs, L. minor is very rare or totally absent. The distribution of L. minor s. 1. is in m o s t continents wider than that of L. gibba, owing to its higher climatic tolerance. The area occupied b y this taxon expands towards moist and cool regions. Rather unexpected is the rare occurrence of L. minor in South America since there exist many regions offering rather favourable climatic conditions. Hegeim~er (1896) mentioned L. minor from O m a s u y o in

361 Bolivia; further, he q u o t e d an unspecified occurrence of this taxon from Chile. Daubs (1965) mentioned Brasilia and Uruguay among the locations, b u t his indications m a y n o t be quite reliable since he reported L. minor even from tropical regions of the Philippines and Malaysia. Van der Plas (1971), in his treatment of the Lemnaceae in "Flora Malesiana" did n o t confirm a single one of these locations. It seems probable that L. minor is more widespread in South America than we might expect from the scanty indications given hitherto in the literature and in herbaria. Within the area o f distribution of L. minor s. 1., L. turionifera grows only in North America and eastern Asia. It endures medium January temperatures of - 2 0 ° C and occurs even in very dry regions. The distribution of L. minor s. str. is probably limited by a January isotherm of a b o u t - 1 0 ° C, b u t this is difficult to deduce from the scarce material we have from northern regions. It seems that L. turionifera is the only species from the group of L. minor that occurs in the northern part as well as in higher mountains of North America. This is probably also true of eastern Asia. L. obscura is confined to moist regions with mild winters and warm summers in the United States. It is distributed along the coast of the Gulf o f Mexico, from the Mexican border to Florida and northwards to northern Texas, Illinois and New Jersey, where it was sporadically noted. In the southern part of this area L. turionifera does not occur and L. minor s. str. is rare. DISCUSSION The distribution of any plant species is limited by its physiological characteristics and b y competition with other species. Physiological limits for the Lemnaceae are influenced by, among other factors, high temperature, low temperature, desiccation, high salinity of waters and low nutrient concentrations. Spirodela polyrhiza, S. punctata (G.F.W. Meyer) Thompson, and Lemna paucicostata grow more rapidly at higher temperatures than do L. gibba or L. minor (Landolt, 1957). On the other hand, S. polyrhiza and L. paucicostata do n o t grow below 13--18 ° C and S. punctata does n o t manifest any growth at 7 ° C. L. gibba and L. minor s. str. will grow at lower temperatures. L. paucicostata can only stand temperatures below 10 ° C as seed. S. polyrhiza and L. turionifera form turions at lower temperatures. The turions sink to the b o t t o m of the water and, therefore, can survive in waters that freeze almost to the b o t t o m in winter. The growth of L. gibba, and, to a somewhat lesser extent, that of L. turionifera, are inhibited in waters with low nutrient content. This is probably w h y L. gibba is restricted to areas that have rather low precipitation during the vegetation season and where nutritive salts are available in higher concentrations. L. paucicostata and L. gibba in the seed state can survive the drying of waters. The greatest competition occurs generally between plants that resemble each other morphologically and have similar growing habits. Competing species

362 of the L. gibba--L, minor group are especially other species of the Lemnaceae, e.g. Spirodela polyrhiza, S. punctata, Lemna paucicostata. Nevertheless, the most intense competition appears to occur between species of the same group. The actual pattern of distribution of the group is determined b y the diversity of physiological characters as well as b y competition from species bccurring within the same area. Newly introduced, or newly differentiating, taxa can only establish themselves in a geographical region if they are at least as competitive as the species already present, or if they are adapted to o c c u p y a different ecological niche. As far as L. minor s. 1. is concerned, L. obscura and L. turionifera are such ecologically specialized types, L. turionifera growing in more continental areas and L. obscura occurring in warmer regions than L. minor s. str. There is also some differentiation within L. gibba s. 1. Distinctly smaller plants known under the names of L. disperma and L. parodiana occur in Australia, California and Argentina. They mostly grow within the areas typical of L. gibba. We could n o t trace any ecological difference between locations of typical L. gibba and those of L. disperma or L. parodiana. However, further studies on this subject are required. Our investigations show that the group of L. gibba--L, minor is very difficult to subdivide morphologically into distinct taxa. Two reasons are principally responsible, as follows: (1} Most of the characteristics are n o t recognizable under all conditions. The most representative features of L. gibba (gibbosity, number of ovules, pigmentation, arrangement of the nerves) m a y only be observed under certain conditions such as climatic setting and (or) chemical composition o f the water. However, these conditions are not yet precisely known. The recognition of the other taxa (e.g.L. turionifera, L. obscura) encounters similar difficulties. (2) There exist certain taxa that combine the characters of both L. minor s. str. and L. gibba s. str. Thus, they obscure the species limits (e.g.L. obscura, L. disperma). Furthermore, transition forms possibly of hybrid origin might occasionally appear, b u t they do not seem to be widely spread. As a consequence, we have to admit that, even for specialists, it is often very difficult to determine plants belonging to the group of L. gibba-L. minor. As in other critical species groups, we are able to recognize a given species only if the plants are in a suitable developmental stage and if the range of variation is verified experimentally. ACKNOWLEDGEMENTS The author gratefully acknowledges the help of his co-workers. Mr O. Wildi carried o u t the water analyses; Miss E. Br~im kept, efficiently and with great patience, our stock collection of the Lemnaceae and also made most of the photographs and graphs. Mr H. Sigg gave technical help. I would particularly like to thank Mrs D. Weber for the translation as well as Dr K. UrbanskaWorytkiewicz for many valuable suggestions during the preparation of the manuscript. Thanks are also due to Dr Th.B. Croat, curator of phanerogams of the Missouri Botanical Garden Herbarium, for the loan of the t y p e specimen of L. minor var. obscura Austin.

363

REFERENCES Daubs, E.H., 1965. A monograph of Lemnaceae. Ill.Biol. Monogr., 34:118 pp. De Lange, L., 1972. A n Ecological Study of Ditch Vegetation in The Netherlands. Thesis, University of Amsterdam, Amsterdam, 112 pp. De Lange, L., 1975. Gibbosity in the complex Lemna gibba--Lemna minor: Literature survey and ecological aspects. Aquat. Bot., 1: 327--332. De Lange, L. and Pieterse, A.H., 1973. A comparative study of the morphology of Lemna gibba L. and Lemna minor L. Acta Bot. Neerl., 22: 510--517. De Lange, L. and Segal, S., 1968. Over het onderscheid en de oecologie van Lemna minor en Lemna gibba. Gorteria, 4: 5--12. Den Hartog, C. and Van der Plas, F., 1970. A synopsis of the Lemnaceae. Blumea, 18: 355--368. Giardelli, M.L., 1937. Una nueva especia de Lemnacea de la Flora Argentina. Notas del Museo de La Plata 2: 97--100. Giardelli, M.L., 1941. Lemna disperma, especia nueva para la Flora Argentina. Darwinia, 5: 190--193. Gray, A., 1867. Manual of the Botany of the Northern United States. Ivison, Phinney, Blakeman and Co., N e w York, N.Y., 5th edn., 479 pp. Harrison, E.D. and Beal, E.O., 1964. The Lemnaceae (duckweeds) of North Carolina. J. Elisha Mitchell Sci. Soc., 80: 12--18. Hegelmaier, F., 1868. Die Lemnaceae. Eine Monographische Untersuchung. Engelmann, Leipzig, 169 pp. Hegelmaier, F., 1871. Die Fructificationsteileyon Spirodela. Bot. Z., 29: 654. Hegelmaier, F., 1896. Systematische Uebersicht iiber die Lemnaceae. Bot. Jahrb., 21: 268--305. Hicks, L.E., 1932. Ranges of p H tolerance of the Lemnaceae. Ohio J. Sci., 32: 237--244. Kandeler, R., 1975. Species delimination in the genus Lemna. Aquat. Bot., 1: 365--376. Landolt, E., 1957. Physiologische und ~kologische Untersuchungen an Lemnaceen. Ber. Schweiz. Bot. Ges., 67: 271--410. Luther, H., 1951. Die Verbreitung hSherer Wasserpflanzen im brackischen Wasser Finnlands. Acta Bot. Fenn., 50: 180--187. McClure, J.W. and Alston, R.E., 1966. A chemotaxonomic study of Lemnaceae. Am. J. Bot., 53: 849--860. Pieterse, A.H., 1975. Physiological, morphological and anatomical aspects of gibbosity in Lemna gibba. Aquat. Bot., 1: 333--344. Pieterse, A.H., Bhalla, P.R. and Sabharwal, P.S., 1970. Control of gibbosity in Lemna gibba G3 by ethylenediamine-di-O-Hydroxyphenylacetic acid (EDDHA). Acta Bot. Neerl., 19: 521--524. Spohr, E., 1926. Uber das Vorkommen yon Sium erectum Huds. und Lemna gibba L. in Estland und fiber deren nordSstliche Verbreitungsgrenzen in Europa. Acta Horti Bot. Univ. Latviens., 1 : 2 2 pp. Van der Plas, F., 1971. Lemnaceae. Flora Malesiana, Ser. I. Spermatophyta, 7: 219--237. Walter, H. and Lieth, H., 1967. Klimadiagramm-Weltatlas. Fischer, Jena. Wol'ek, J., 1974. A preliminary investigation on interactions (competition, allelopathy) between some species of Lemna, Spirodela and Wolffia. Ber. Geobot. Inst. Eidg. Techn. Hochsch. Stift. Riibel, Ziirich, 42: 140--162.