Quiescence, growth and senescence of Egeria densa in Lake Marion

Aquatic Botany, 20 (1984) 329--338

329

Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

QUIESCENCE, GROWTH AND SENESCENCE OF EGERIA DENSA IN LAKE MARION

K.D. GETSINGER* and C.R. DILLON

Botany Department, Clemson University, C/emson, SC 29631 (U.S.A.) (Accepted for publication 11 September 1984) ABSTRACT Getsinger, K.D. and Dillon, C.R., 1984. Quiescence, growth and senescence of Egeria densa in Lake Marion. Aquat. Bot., 20: 329--338. Seasonal changes in biomass production and morphology of the submersed vascular plant Egeria densa Planchon (Brazilian elodea) were followed in Lake Marion, South Carolina, from March 1980 to May 1981. Biomass maxima occurred in late summer and late fall; these were followed by periods of senescence denoted by biomass loss through sloughing and decay of tips and branches. A period of quiescence was observed in the winter. Rootcrowns and stems containing double nodes were verified as the overwintering and propagative structures. INTRODUCTION

The submersed aquatic macrophyte Egeria densa Planch. (Brazilian elodea), a member of the Hydrocharitaceae, has become a prominent weed in lakes and rivers of the southeastern United States (Solymosy and Gangstad, 1974). Since 1966, the plant has occupied over 10 000 ha of the Santee-Cooper River System in South Carolina, the major portion of which (about 8000 ha) occurs in the upper reaches of Lake Marion (33°34'N, 80°28'W) (Roach, 1977). This large stand threatens reservoir functions which include flood control, electrical power generation, navigation and recreation and has accelerated sedimentation or infiUing (USDA, 1973; Roach, 1977). The purpose of this investigation was to study the life history of the plant and the timing of its growth phases in Lake Marion. The biomass, morphological and phenological data reported will supplement physiological data from a concurrent study. MATERIALS AND METHODS

S t u d y area L a k e Marion is a 39 3 6 6 ha h y d r o - e l e c t r i c reservoir in the S a n t e e - C o o p e r River S y s t e m , l o c a t e d in t h e coastal plain o f S o u t h Carolina a n d f o r m e d b y *Present address: Environmental Laboratory, USAE Waterways Experiment Station, Vicksburg, MS 39180, U.S.A. 0304-3770/84/$03,00

© 1984 Elsevier Science Publishers B.V.

330 the i m p o u n d m e n t of the Santee River in 1941. It has a mean depth of 4 m and a mean hydraulic retention time of 44 days (Roach, 1977). The upper reaches contain thousands of hectares of shallow water conducive to aquatic plant growth. A 5-ha site, with a mean depth of 1.5 m at the upper end o f the lake was selected as the study area. It contained an almost monospecific stand of Egeria bounded on the shore side by swamp forest. A narrow band of Ludwigia uruguayensis {Camb.) Hara (waterprimrose) extended from the forest into the fringe o f the bed. Isolated shoots of the submersed species Ceratophyllum demersum L. (coontail) and Najas guadalupensis (Sprengel) Magnus (bushy pondweed) occurred sporadically t h r o u g h o u t the stand. Scattered patches of the filamentous green alga Oedogonium sp. were observed entangled in the submersed macrophyte mats during late spring, and epiphytic, globular, gelatinous masses of the c y a n o p h y t i c Gleotrichia sp. occurred during late summer and early fall. Precipitation, river input and spillway o u t p u t caused fluctuations to 0.5 m in water level.

Pheno-morphological determination Field measurements and collections were made 1 day each m o n t h from June 1980 to May 1981, except February, to determine canopy height and the general morphology and condition of the plants. Ten samples of entire plants (shoots, rootcrowns and roots) were removed from the substrate by a scuba diver or by the use of a long handled rake operated from a boat. There were no discernable differences in samples collected by either of these methods. Collections were place in ice chests containing lake water for transport to the laboratory. Stems (shoots from the rootcrown) and branches (all other shoots) which were necrotic, with deteriorated leaves or w i t h o u t apices, were classified as " a g e d " , and green shoots and branches with healthy apices as " n e w " . Roots were not categorized since no clear distinction could be made. Measurements were made of old and new growth per rootcrown, and the number and length of stems, primary (1°), secondary (2°), tertiary (3 °) and quaternary (4 °) branches and of roots. Primary branches arise from stems, 2 ° branches from 1 ° branches, 3 ° from 2 °, etc.

Biomass determination Ten replicate samples for biomass determinations were collected on 1 day each m o n t h for 14 m o n t h s (March 1980 to May 1981, except February) by use of a GrCntved sampler (GrC~tved, 1957) (area = 464 cm2). Plants were harvested at approximately 10-m intervals, sealed in plastic bags, packed in ice for transport to the laboratory and were analysed within 36 h. The plants were washed to remove any adhering sediment (copropel) and separated into shoots, rootcrowns and roots, centrifuged in a top-loading washing machine on spin cycle for 10 min, and weighed. Fresh weight to dry weight conversions were determined from 20 to 25 g subsamples of shoots, and 1 to 10 g

331

subsamples of rootcrowns and roots were taken from each sample and oven dried (70°C) to constant weight. Dried materials were ground in a Wiley mill (40 mesh) and 0.5 g combusted in a muffle furnace at 550°C for 4 h to determine ash weight. RESULTS

Pheno-morphology Monthly growth data are given in Fig. 1 as the product (numbers X lengths in cm) of mean numbers and mean lengths of roots, main stems and l°--4 ° branches. Four definitive growth phases were recognized in Lake Marion: Summer (June 1980--September 1980); Autumn (October 1980--December 1980); Winter (January 1981--March 1981); Spring (April 1981--May 1981).

DATE MAY81 829.8 APR81

MAR81

JAN81 DEC80

NOVBO 553.1

OCTBO SEP80

JUL80

JUNS0

i~" 94.8 ~ AGED

553.4_ Z NEW GROWTH

624.9 / ROOTS

Fig. I. Monthly growth data charted as the product of m e a n numbers and m e a n lengths (in cm) of aged and n e w -- from the bottom: main shoots (solid black), I ° branches (cross hatched), 2 ° branches (hatched right), tertiary branches (empty), quaternary branches (hatched left) and roots (hatched left).

Summer phase Summer plants comprised both aged stems {branches had deteriorated) and new parts produced in the spring and summer of 1980. The number of

332

aged stems diminished rapidly during this phase and all disintegrated by September. In June, new growth consisted of stems with 1 °, 2 ° and 3 ° branches. Quaternary branching occurred from July t h r o u g h September. The numbers and lengths of roots remained fairly stable t h r o u g h o u t summer while the numbers of new stems increased from 4 to 6.1 per rootcrown. The total numbers of branches reached a peak in August at 14. This was followed by a slight decline to 12.8 branches in September. Simultaneously, stem lengths increased from an average of 95.1 cm in June to 123.3 cm in July, then decreased to 91.5 cm in September. Change in length of new branches (4--47 cm) was considerably less than that of stems, although the length of both increased in June, reached a maximum in July, and then decreased in September due to sloughing or fragmentation. During this late summer senescence, surface water temperature was greater t h a n 30°C and masses of branches within this upper stratum deteriorated.

Autumn phase A u t u m n was characterized by the p r o d u c t i o n of new branches from summer stems and of new stems from the rootcrowns. There was a concurrent decline in the numbers and lengths of aged stems and branches. Aged stem lengths were reduced from 75.7 cm in October to 55.5 cm by December. A similar reduction was observed in lengths of all aged branches and by December aged 3 ° and 4 ° branches had disappeared. The numbers of new 1 ° branches were approximately 7 per rootcrown in November and December. New 2 ° branches stabilized at 3, and 3 ° declined to 1 per rootcrown, while new 4 ° branches were rarely produced during this period. However, new stems and branches exhibited increases in length. Decreases in numbers and lengths of aged stems and branches were indicative of plant disintegration and fragmentation associated with fall senescence. Root lengths were slightly less than observed earlier and remained stable during the period.

Win ter phase Winter was marked by the proliferation of new, short stems to an average of 9.9 per rootcrown. Numbers of 3 ° branches continued to decline and by March only 1 ° and 2 ° branches were present. Stems and branches were reduced in length by 20--25% during this period, while r o o t numbers reached the highest value recorded for the study at 64.3 per rootcrown.

Spring phase Spring was marked by an acceleration of growth. Aged parts, which, as defined, consisted of necrotic, tipless remnants deteriorated rapidly throughout the period and by May only stems and 1 ° branches remained. New

333

growth, comprising stems and branches with intact apices produced in the winter and in the current period, increased in both numbers and length, while roots decreased in number, but increased in length. Prior to penetration of the sediment, roots produced from elevated double nodes were devoid of root hairs which were produced subsequently. Stand biomass

Biomass in the stand reached 2 maxima (Fig. 2). Mean dry weight increased from 77.4 g m -: in March to 373.9 g m -~ in July. This was followed by a period of senescence that resulted in a decrease of more than 53% by October. Recrudescence occurred in November and December, producing another peak of 276 g m -: in December. Winter quiescence plus loss by fragmentation then resulted in a reduction to 101.3 g m -: by the following March although, by May, biomass was comparable to that measured in April of the previous year. Stems, branches and leaves, rather than rootcrowns or roots, comprised the largest proportion (90.5% + 7.4) of plant material collected throughout the study. BOO

4.0

8.6

6.3

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Fig. 2. Monthly biomass means (dry wt.) compartmentalized - - f r o m the bottom: root (cross hatched), rootcrowns (empty), and stems including branches (hatched right). The empty boxes atop the bars represent 95% confidence intervals. The numbers above the bars are root/stem percentages.

334

Percentage dry weight and ash content Dry weight as a percentage of fresh weight fluctuated slightly t h r o u g h o u t the study. The average was 8.9% + 1.7, with a m a x i m u m of 13.4% in summer and a minimum of 6.1% in spring. Conversely, ash as a percentage of dry weight averaged 20.1% ± 4.9, with a m i n i m u m of 11.9% in summer and a m a x i m u m of 28% in spring (Fig. 3).

g ~SH ~T.

J

g DRY lrr.

.........

~/

a..

i ......... ! ......... i ......... i ......... i" . . . . APRIO NAYBO OULIlO SlEPSO OCTOO

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~1 ......... ! MARSt MAYO1

MONTH Fig.

3. Plot

of

the percentage ash and the

percentage

dry

weight

of stems.

Canopy height There were m o n t h l y fluctuations in the height of the canopy above the b o t t o m of the study area (Table I). These correlated fairly well with biomass observations (r = 0.86). The periods when the canopy surfaced in August (height = 1.5 m), or was found near the surface in December and January, reflect biomass maxima. TABLE

I

Canopy

height

above

the bottom

throughout

the year.

Mean

water

depth

was 1.5 m

Date

Height

(m)

30

21

11

9

25

23

21

20

17

22

4

2

5

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Jan

Mar

Apr

May

0.10

0.23

1.25

1.40

1.50

1.30

0.40

1.00

1.30

1.30

0.20

0.30

0.35

335 DISCUSSION

Plant description and general life cycle In Lake Marion, Egeria densa grows as a submersed, r o o t e d perennial in depths up to 3 m. Both stems and leaves function as photosynthetic structures. Blackburn et al. (1976) reported that the o p t i m u m growth conditions occurred fromApril to September in the southeast of the U.S.A. and that the plant "dies b a c k " to the rootcrowns during the winter months. We f o u n d that the plant overwinters along the b o t t o m in a green condition. Flowering, which varies in intensity from year to year, is initiated in late May and followed by 2 maxima, 1 in early June and another in September. When the plant grows to the water surface, spathes are produced which in turn produce 2--4 white, tri-petalous, estaminate flowers, with 9 yellow anthers and a central nectary. These are elevated several centimeters above the water on a thread-like h y p a n t h i u m (Fig. 4). Morphology of flowers from Lake Marion fits the description of staminate flowers given b y St. John (1961). No pistillate flowers, fruits or seeds were observed. Leaves are usually arranged in whorls of 4, although whorls of 3 or 5 are occasionally present. Nodes are regularly spaced b u t internodes are longer in older stems.

Root

Fig. 4. M o r p h o l o g i c a l characteristics o f the f l o w e r and r o o t c r o w n o f Egeria densa.

During the months of late May--August, profuse branching (usually 50 cm above the substrate) forms a t y p e of canopy which is f o u n d in some other submersed species such as Myriophyllum spicatum L. (Adams et al., 1974; Grace and Tilly, 1976) and Hydrilla verticillata (L.f.) Royle (Haller and Sutton,

336

1975). In August proliferated branches lie intertwined on the water surface to form vast, dense mats that can cover hundreds of hectares and persist until senescence in the fall. Specialized meristematic regions, described b y Jacobs (1946) as double nodes, are located at 6--12 nodal intervals along stems or branches. A double node (Fig. 5) actually consists of 2 nodes that are virtually superimposed. Occasionally, double nodes may comprise nodes that are separated by internodal lengths of 1--5 mm. King (1943) and Jacobs (1946) have shown that these regions are of primary importance in branching and in vegetative propagation, for it is from this region that a bud and adventitious roots are initially produced (Fig. 5); they also showed that stem fragments which contain double nodes can develop into new plants, a characteristic that led King to refer to double nodes as bud nodes and single nodes as pseudo-nodes. Our own unpublished experiments have shown that superimposed, double nodal fragments must be at least 7.5 mm in length to p r o d u c e roots and stems. Shorter fragments invariably disintegrated as did all fragments lacking such nodes.

'al ;h

Dooble

Node

/ktv~tili Sir

Fig. 5. Morphological characteristics o f the s t e m o f Egeria densa.

While t h e y may arise from viable stem fragments that have settled to the b o t t o m , new rootcrowns (Fig. 4) develop principally from one to several double nodes along an aged, prostrate stem, that has sunk to the b o t t o m , but is still connected to an older rootcrown. Growth appears stoloniferous until the senescent stem disintegrates. R o o t c r o w n s eventually b e c o m e a mass o f meristematic tissue that produces numerous stems and roots.

337 The presence o f new shoots and branches in January and March indicates that growth was continuous, although the rate was much slower than in other phases. This we considered to be a period of quiescence. True winter d o r m a n c y (cessation of growth) was not observed. Kunii (1981) reported that in Japan Elodea nuttaUii (Planch.) St. J o h n also lacked a period of winter d o r m a n c y and exhibited slow growth at temperatures near 4°C. The bimodal biomass curve in Lake Marion has been observed in other species of submersed macrophytes in temperate lakes. Menzie (1979) reported 2 biomass peaks (July and October) for Myriophyllum spicatum in the Hudson River, New York, as did Chapman et al. (1974) for CeratophyUum demersum in December--January and in June in Lake Ohakuri, New Zealand. Tanimizu and Muira (1976) reported a fluctuating standing crop for E. densa in Lake Biwa, Japan, with a maximum in March, a decline until June, then a continued growth into the following January that produced a standing crop double that of the preceding February. The latter observations were made under an annual temperature regime very similar to that observed in our study. Barko and Smart (1981) were able to significantly reduce biomass production in growth chamber experiments with Egeria densa b y raising temperatures to 32°C. In more recent studies, of the interactive effects of constant levels of light and temperature, Barko et al. (1984) have shown that in Elodea canadensis at a b o u t 30°C production of shoot mass is reduced at low, medium or high light intensities. We are of the opinion that these are the major contributing factors to the A u t u m n senescence observed. We recorded the cessation of terminal growth, the deterioration of surfaced branches, and resultant reduction in biomass when surface temperatures rose to more than 30°C. Growth resumed as temperatures fell below 30°C in the fall, and the late fall biomass peak was recorded when the water temperatures had reached approximately 10°C, below which growth slowed perceptibly. These temperature-triggered p h e n o m e n a are identical to "heat and cold rigor" postulated b y Setchell (1929) for Zostera marina L. The dramatic reduction of biomass which followed t h e drop in water temperatures in early December characterized the period of quiescence. Rapid water flow through the reservoir at the end of winter accelerated sloughing and fragmentation and contributed to this substantial loss. The percentage of root biomass {Fig. 2) was higher in the spring than in summer because of the loss of stems and branches during quiescence and then subsequent production. The inverse relationship of percentage dry weight to percentage ash indicates the minor importance of mineral assimilation in causing biomass variations and suggests the accumulation of organic compounds. This was borne o u t in a concurrent study (data not provided) in which starch was shown to comprise 50% of the dry weight of summer stems.

338 CONCLUSIONS T h e success o f Egeria in S o u t h Carolina is a f u n c t i o n o f its ability t o rep r o d u c e vegetatively b y m e a n s o f specialized s t r u c t u r e s such as r o o t c r o w n s or d o u b l e n o d e s , and t o initiate a g r o w t h r e s u r g e n c e f o l l o w i n g sloughing a n d f r a g m e n t a t i o n i n d u c e d b y e x p o s u r e t o the stress o f elevated s u r f a c e w a t e r temperatures. REFERENCES

Adams, M.S., Titus, J. and McCracken, M., 1974. Depth distribution of photosynthetic activity in a Myriophyllum spicatum community in Lake Wingra. Limnol. Oceanogr., 19: 377--389. Barko, J.W. and Smart, R.M., 1981. Comparative influences of light and temperature on the growth and metabolism of selected submersed freshwater macrophytes. Ecol. Monogr., 51: 219--235. Barko, J.W., Hardin, D.G. and Matthews, M.S., 1984. Interactive influences of light and temperature on the growth and morphology of submersed freshwater macrophytes. Technical Report A-84-3, U.S. Army Engineer Waterways Experiment Station, CE, Vicksburg, MS. Blackburn, R.D. and Gangstad, E.O., 1976. Efficacy and residues of diquat applied for control of Egeria and Hydrilla. In: Aquatic Use Pattern for Diquat for the Control of Egeria and Hydrilla. Tech. Report 13, USAEWES, Vicksburg, pp. C3--C25. Chapman, V.J., Brown, J.M.A., Hill, C.F. and CarL J.L., 1974. Biology of excessive weed growth in the hydroelectric lakes of the Waikato River, New Zealand. Hydrobiology, 44 : 349--363. Grace, J.B. and Tilly, L.J., 1976. Distribution and abundance of submerged macrophytes, including Myriophyllum spicatum L. Angiospermae, in a reactor cooling reservoir. Arch. Hydrobiol., 77: 475--487. Gr~tved, J., 1957. A sampler for underwater macrovegetation in shallow water. J. Cons. Int. Explor. Mer., 22: 293--297. Hailer, W.T. and Sutton, D.L., 1975. Community structure and competition between Hydrilla and Vallisneria. Hyacinth Contr. J., 13: 48--50. Jacobs, D.L., 1946. Shoot segmentation in Anacharis densa. Am. Midl. Nat., 35: 283-286. King, L.J., 1943. Responses in Elodea densa to growth regulating substances. Bot. Gaz., 105: 127--151. Kunii, H., 1981. Characteristics of winter growth of the detached Elodea nu ttallii (Planch.) St. John in Japan. Aquat. Bot., 11 : 57--66. Menzie, C.A., 1979. Growth of the aquatic plant Myriophyllum spicatum in a littoral area of the Hudson River estuary. Aquat. Bot., 6: 365--375. Roach, H.B., 1977. Long term management plan for aquatic plant control in the SanteeCooper Reservoir. South Carolina Public Service Authority, Mimeo Report, Moncks Corner, 60 pp. SetcheU, W.A., 1929. Morphological and phenological notes on Zostera marina L. Univ. Calif. Publ. Bot., 14: 389--452. Solymosy, S.L. and Gangstad, E.O., 1974. Nomenclature, taxonomy and distribution of Egeria and Elodea. Hyacinth Contr. J., 12: 3--5. St. John, H., 1961. Monograph of the genus Egeria Planchon. Darwiniana, 12: 293--307. Tanimizu, K. and Muira, T., 1976. Studies on the submerged plant community in Lake Biwa. 1. Distribution and productivity of Egeria densa, a submerged plant invader, in the South Basin. Physiol. Ecol., Japan, 17: 283--290. Translation by M. Tokeshi, 1983. USDA, 1973. Santee River Water and Land Resources: North Carolina, South Carolina. Economic Research Service, Forest Service, Soil Conservation Service, U.S. Dept. of Agric, Washington, D.C., 272 pp.