- Email: [email protected]
Growth and production of Lagarosiphon ilicifolius in Lake Kariba — a man-made tropical lake
Aquatic Botany, 37 ( 1 9 9 0 ) 1-15
1
Elsevier Science Publishers B.V., A m s t e r d a m - - P r i n t e d in T h e N e t h e r l a n d s
Growth and production of Lagarosiphon ilicifolius in Lake Kariba a man-made tropical lake
C e c i l M a c h e n a 1, N i l s K a u t s k y 2 a n d G u n i l l a L i n d m a r k 3
~Lake Kariba Fisheries Research Institute, P.O. Box 75, Kariba, Zimbabwe and lnstitute of Ecological Botany, Uppsala University, P.O. Box 559, S-751 22 Uppsala (Sweden) 2Ask~ Laboratory, Institute of Marine Ecology and Department of Zoology, University Stockholm, S-106 91, Stockholm (Sweden) 31nstitute of Limnology, University of Lund, Box 65, S-221 00, Lund (Sweden) (Accepted for publication 31 October 1989)
ABSTRACT Machena, C., Kautsky, N. and Lindmark, G., 1990. Growth and production ofLagarosiphon ilicifolius in Lake Kariba - - a man-made tropical lake. Aquat. Bot., 37:1-15.
Two different methods, the diurnal oxygen curve method in plexiglass enclosures, and the incremental growth technique were used to complement production estimations ofLagarosiphon ilicifolius Oberm. in Lake Kariba. The incremental growth technique gave a production rate of 16.4 mg g - ~dry weight ( D W ) d a y - ~ (7.5 mg C g - ~ DW d a y - t ) which was 6.5 times higher than the rate of 1.16 mg C g - ~ DW d a y - ~obtained for the community from the diurnal oxygen curve method. The difference is largely accounted for by the total respiration of the community, which is inherent to the enclosure technique, and also by the fact that the measurements were carried out for short periods of time. Using the production rate from growth measurements, the biomass production of Lagarosiphon was calculated as 1.6 g DW m -2 d a y - ~and to 598.6 g m -2 year- 1. The average community P / R ratio of 1.16 indicates that the community is operating close to steadystate, and shows a high degree of self maintenance. Lagarosiphon has an annual turnover rate of 2.4 but the populations are perennial (i.e. grow all year round). The main growing season is in summer, from October to February. Cohorts that develop during the summer, branch extensively at the end of this growth period, and while occluding light to the bottom, die off in the process. The resulting drifting mats fragment and constitute the major reproductive modules. Although flowering was observed, sexual reproduction does not appear to be important. It is concluded that the difference in the production values between the community taken as a whole and individual plants reflects the role different components of the ecosystem play in the metabolism of the macrophyte community. For this reason the value of 16.4 mg g-~ day-~ calculated from marked individuals is a more realistic growth rate of Lagarosiphon plants in this study.
0304-3770/90/$03.50
© 1990 Elsevier Science Publishers B.V.
2
C. MACHENA ET AL.
INTRODUCTION
This study was carried out to estimate the productivity of a Lagarosiphon ilicifolius Oberm. dominated c o m m u n i t y and to follow the growth and phenology of Lagarosiphon in Lake Kariba. A number of standard methods for primary production measurements have been r e c o m m e n d e d (Vollenweider, 1974; Kemp et al., 1986). In the present study we use two of them: changes in growth over time in marked plants, and in situ studies of oxygen production and its seasonal variation in plexiglass enclosures. Benthic macrophytes (i.e. macrophytes living on the bottom of the lake) form productive communities (Cattaneo and Kalff, 1980; Morgan and Kitting, 1984) and are important for fisheries. Their contribution to the total biomass production is generally related to the size and morphometry of the water body. For some shallow lakes e.g. Swartvlei (Howard-Williams, 1978 ) and Lake Chad (L6v6que et al., 1983 ) hydrolittoral (i.e. the zone extending from the water-line to the depth at which plants are rooted) production exceeds pelagic planktonic algal production. However, for deeper lakes the opposite usually holds. Benthic macrophytes are also important in the lake as a substrate for microand macrofauna and epiphytic algae (McLachlan and McLachlan, 1971; Wetzel & Hough, 1973; Pelican et al., 1978; Howard-Williams and Allanson, 1981; Morgan & Kitting, 1984; Carpenter and Lodge, 1986). Machena and Kautsky ( 1988 ) argued that the development of the submerged vegetation in Lake Kariba facilitated the development of other benthic communities, particularly gastropods and bivalves. As Lagarosiphon is the dominant species regarding both biomass (Machena and Kautsky, 1988) and area covered (Machena, 1987), production studies on this species may give an indication of the role of macrophytes in the ecology of the lake. MATERIAL AND METHODS
Study area Lake Kariba (16028 ' to 18°06'S; 26004 ' to 2 9 ° 0 3 ' E ) is an artificial lake formed after d a m m i n g of the Zambezi River. It is located in Southern Africa between Zambia and Zimbabwe and is the third largest man-made lake in the world. Its features and morphology are presented in Table 1. The main axis of the lake has a SW-NE orientation following the old Zambezi River basin. (For details see Balon and Coche, 1974). Two sites were chosen, one close to the Fisheries Research Institute at the eastern end of the lake where c o m m u n i t y metabolism studies were carried out
LAGA I~OSIPHON ILICIFOLIUS IN LAKE KARIBA
3
TABLE 1 Main features and morphology of Lake Kariba at a water level of 485 m a.s.1. Partly recalculated from Balon and Coche (1974), and potential colonisable areas of submerged macrophytes Length Width (mean) Depth (mean) Depth (maximum) Area Average bottom area per 1 m depth interval between 0-15 m Total bottom area between 0 and 5 m deep Volume Percentage of bottom area between 0 and 15 m deep Total length of shoreline
277.0 19.4 29.2 120.0 5364.0
km km m m km 2
105.2 km 2 m 526.1 km z 156× 109 m 3 23.5% 2668.0 km
and the other half-way along the Zimbabwean side of the lake where the growth of individual plants was followed. Site 1 is on an exposed shore, which is regularly subjected to turbidity from wave action. Studies at the site were carried out at a depth of 1 m. Site 2 was situated 4 m deep and about 1 km offshore. The standing crop of Lagarosiphon was similar at both sites and also similar to the mean standing crop for the lake within the colonised zone between depths of 0 and 5 m (Machena and Kautsky, 1988).
Measurement of growth rates Growth rate was measured on individually marked Lagarosiphon ilicifolius plants that had grown from fragmented shoots. In October when the plants were small (unbranched with an average length of 20 _+2.65 cm), a total of 40 plants in 4 (0.5×0.5 m ) quadrats were individually marked. Pieces of steel rods were pushed into the ground alongside each identified ramet (Harper, 1977) to distinguish these from plants that would establish later during the study. The positions of the plants in each quadrat were then marked on roughened plastic sheets (for use under water) on which all data were recorded. The marked plants were assumed to be of the same age and are treated as one cohort. The total length of each shoot and its branches were measured in cm once every m o n t h from October 1986 until the plants senesced in April 1987. Lagarosiphon is rooted and grows vertically with little branching until it reaches close to the water surface where it branches extensively thereby in-
4
C. MACHENA ET AL.
creasing its photoreceptive surface area. A length:weight regression was calculated using plants collected from the same population as the marked plants Y= 3 . 0 4 X - 5.5
( n = 36; r2=0.96)
(1)
where Y= dry weight (mg) and X = total length of shoot and branches (cm). This equation was used to calculate the weight increments for each month. Relative growth rates were calculated using Eqn. (2) as outlined in Hunt (1978) R-
log~ W2- log~ Wl
T2- T,
(2)
where W1 is dry weight in g at time T1 in days and W2 is dry weight at time T2 and e is the base of the natural logarithm. The mineral ash (inorganic) content of the plants, which amounted to 17.5%, (as measured once in the early part of the study) was subtracted from the weight increments. This provided values for changes in the organic weight (Hunt, 1978) expressed per unit dry weight of the plant biomass and was found to be similar to the value of 15% reported for Ceratophyllum demersum L. by Lipkin et al. (1986). Areal photosynthetic rates were calculated using Eqn. (3):
Pr=CO mgg -1 day-1 × B
(3)
where Pr= areal production; C = changes in organic weight per unit weight of plant per unit time (rag g-~ day -1 ); B=biomass (g DW m -2) of Lagarosiphon. Changes in weight in this paper refer to organic weight. The carbon content of Lagarosiphon was assumed to be 46% of the total organic weight (ash-free DW) (Davies, 1970; Westlake, 1965 in Solander, 1982); the ash content was determined by ignition in a muffle oven at 550°C. Denny ( 1985 ) gives the carbon contents of leaf tissues ofPotamogeton pectinatus L. between 42 and 49%. Annual variation in the carbon content of the plants was assumed to be insignificant (Solander, 1982 ).
Measurement of community metabolism Oxygen production and consumption The community metabolism of Lagarosiphon was calculated using diurnal oxygen curves as described in Jansson and Wulff ( 1977 ) (see also Dybern et al., 1976 ). The communities were enclosed in plexiglass cylinders in situ with a lid on top, which enclosed a surface area of 0.066 m z and a water volume of 22.4 1. The lid had two outlets, one for withdrawing water samples and the other one for inserting the oxygen probe. The cylinder was pushed gently into the substrate to ensure a substrate seal and was held in position by four steel bars to prevent tipping of the cylinder from wave action.
5.9 7.3 9.0 2.9 3.8 8.7 8.7
cylinder (g DW)
Lag. in
19.93 30.9 31.7 29.6 24.75 22.9 9.48
(7.49) (11.6) (11.9) (11.13) (9.30) (8.61) (3.56)
Gross production ~ (GP: mg 02 g- ~day- ~)
1.78 (0.67) 3.4 (1.3) 4.31(1.6) 1.30(0.49) 1.19 (0.44) 3.02 (1.11) 1.24 (0.47)
Areal 2 Gross production (A/~. g 02 m -2 day- t ) 1.55 3.1 6.1 1.8 0.96 1.7 1.33
(0.58) (1.2) (2.3) (0.41) (0.37) (0.6) (0.50)
Areal 2 community respiration (AR:gO2m-2day -l) 0.98 0.9 -4.9 4.86 3.1 3.6 -0.24
Net community production (PN:mgCg-lday -l)
17.31 28.4 44.9 16.66 16.68 13.09 10.12
(6.51) 1.15 (10.7) 1.09 (16.8)0.71 (6.27) 1.20 (6.2) 1.24 (4.92) 1.77 (3.80) 0.93
Community respiration AP/AR (CR:mgO2g-lday -t)
tProduction or respiration values per unit weight of plant obtained by dividing changes in oxygen levels in the enclosure by the weight of plant harvested in the enclosure. 2Areal values of production and respiration obtained by extrapolating total values within the enclosure to m 2. 3Refers to Fig. 3; Lag. =L. ilicifolius.
A23-25/I1/85 B26-28/01/86 C15-17/02/86 D10-12/05/86 E 07-09/06/86 F26-28/07/86 G 15-17/03/88
Period of study 3
Lagarosiphon ilicifolius community metabolism in plexiglass enclosures. Carbon equivalents of production and respiration values are given in parentheses
TABLE 2
:m
t'rl
7~
6
C. MACHENA ET AL.
Diurnal measurements were begun at dusk and continued for about 37 h, thus covering a full day and the nights before and after. A battery powered bilge p u m p stirred water within the cylinder either continuously or at intervals. Dissolved oxygen and temperature readings were taken every hour using a Yellow Springs 58 oxygen meter with a combined oxygen and temperature probe. At the end of each experiment (carried out during the periods indicated in Table 2 ), the enclosed plants and animals were collected, separated by species and dried to constant weight. Oxygen production and consumption were calculated from diurnal oxygen mass time curves. The respiration rate was calculated as the best fitting slope on night consumption. This was extrapolated to 24 h to obtain total daily respiration. When the best fitting slope on night consumption was continued, the height between this slope and the mass time curve after 24 h of incubation, gave daily gross oxygen production. C o m m u n i t y production and consumption rates were calculated on a unit area basis. As Lagarosiphon was the dominant producer, production and consumption rates were also calculated on a Lagarosiphon unit weight basis.
pH, conductivity, turbidity and light measurement The physical parameters pH, conductivity, turbidity and photosynthetic active radiation (PAR), were measured in the enclosure to help elucidate biological and physical processes in the enclosures. Water samples were taken from the lake m e d i u m and siphoned from the experimental cylinders every 3 h and pH, conductivity and turbidity were measured immediately. Conductivity was determined with a portable Crison meter (model 523) and pH was measured with a Crison portable pH meter 506 and a combined pH electrode. Turbidity was measured as N T U (normal turbidity units ) with a Hach model 16 800 portable turbidimeter. Light penetration (photosynthetic active radiation PAR, 400-700 n m ) adjacent to and at about the centre of the cylinders was measured with a LI-COR- 188B integrating q u a n t u m sensor (submersible) and meter. Total daily PAR was derived by planimetric integration of hourly PAR values. RESULTS
Growth measurement The growth curve (DW) and phenology of individual shoots of Lagarosiphon are shown in Figs. 1 and 2. The plant weight increased rapidly from a mean of 61.6 mg per shoot in October to a mean of 225 mg per shoot in February, when the shoots matured. The production rate was consistently high between October and January when flowering and rapid branching occurred. By February the shoots were
7
LAGAROSIPHON ILICIFOLIUS IN LAKE K A R I B A
300-
-]00 DEATH
1
250~200-
FLOWERING/
?,
u}
60
BRANCHING|/
150-
100-
20
50-
l
ASO
l
i
N
,
i
DJ
i
r
t
,
F M A M J
Fig. 1. Growth of Lagarosiphon ilicifolius L. in Lake Kariba. The onset of branching and death is indicated. Vertical bars are SE of means.
BRANCHING AND FLOWERING
DRIFTING FRAGMENTS
WATER SURFACE 120'
I--r ~" 100' z k0 o -r 80 u~ 60
4020-
( O
N
F
M
Fig. 2. A diagrammatic representation of the growth cycle of Lagarosiphon Kariba showing a marked density of mature shoots at the water surface.
ilic(folius in Lake
8
C. MACHENA ET AL.
extensively branched and attained a m a x i m u m length of 160 cm. Senescence began in February, as evidenced by shoots rotting from the substratum, and by April all plants were detached or dead. As the marked shoots were assumed to be of the same age, the growth period of the cohort can be estimated at 5 months. As the Lagarosiphon populations are perennial in Lake Kariba, this gives a turnover of 2.4 for overall annual net production. Rich et al. ( 1971 ) reported an annual turnover of 1.5 and 3.0, using two different techniques for macrophytes in a Michigan marl lake, and projected a possible range of 0.5 to 5 for macrophytes in general. The mean net production rate for measurement of individual shoots was 16.4 mg g-~ DW day-1. By dividing the daily production rate by l0 (hours of day- light), the hourly value of 1.7 mg g-1 DW was obtained. In terms of net carbon production this is equivalent to 7.5 mg C g-~ DW day-1. Calculations of areal production rate were made using a mean biomass of Lagarosiphon of 100 g m -2 (for the colonised zone of 0-5 m water depth given in Machena and Kautsky ( 1988 ). A mean areal production rate of 1.6 X 103 mg DW m -2 day -1, equivalent to 754 mg C m -2 day -1 was obtained.
Community metabolism The in situ enclosure experiments were performed during different seasons (Table 2 ) to cover variation in environmental conditions and development phases of Lagarosiphon (Fig. 3 ). The diurnal changes in pH, PAR, turbidity, temperature, conductivity and dissolved oxygen are presented in Fig. 3 A-G. As expected, values for temperature, pH and oxygen were lowest in the early morning and peaked late in the afternoon, reflecting normal physical and biological activity. The pH varied by 0.5-1.3 units during 24 h and the total pH span was 6.7-9.5. The increase in pH during photosynthesis is due to the utilisation of carbon dioxide in the production process. The diurnal amplitude for water temperature was 2 °-4 °C and the total temperature range covered by the experiments was 22 °33°C. Conductivity values ranged between 109 and 145/t S c m - 1 during the day. The changes in conductivity are more complex and less consistent, as several interlinked factors and c o m m u n i t y components are involved in the mineralisation process. PAR varied irregularly and was inversely related to turbidity (Fig. 3 ). However, the low PAR values in the early part of the incubation obtained in March ! 988 were due to the light sensor being shaded by vegetation. From variations in the oxygen production and consumption in the enclosure experiments, values for gross production and c o m m u n i t y respiration have been estimated (Table 2). The variation in the weight of the plants in different enclosures was considered when calculating the production and res-
9
LAGAROSIPHON ILICIFOLIUS Ie LAKEKARIBA T C
o:
p} ,'CONDUC-
6 30
~-..~
i~//~__~...~
4 28
~
"
~z ~ ~-,
2 26
" 120
160.20 801 I0
A
1oo
8 F29 6 r28 4 27
110
'20
2 26
,10
6
~-.........
Ft 8
30
100
/---\
6 29
- - __
i150 140
\/
4 28
20
2 27
'10
f
130
112° /
C
.
.
.
9. 29
"Jl
8.28
.-~jr-~i
.
.
.
71110
./,~'~ ~ \
120 ~
~
110
6' 27
8 100 20
4" 2 6
90
10 ,:'
,
.
7 80
10" 27 8" 26
130
6 25 4 24
i 20 - - ' - - -
2 23 E
-
....
~C~
--
10
.,:,~', ~: , c . ,
12 26 10 25
~
8-24
.
8 120 "110 "100 , 7 "90
12 130 11 120
/
6.23
10 110 9 100
4 "22 2.21
F TEN"~RATURE
pH
---- CONDUCTIVITY
PAR
TURBIDITY
I
~. . . .
__ 6.2e
120 10
. " : ! ,: ?~,.,
~
"""~'--.~'~""
427
~
------...
----~
/~
: : :
226
20 0
.<;i:...
G i
18
24
06
12
18
8 90
7 80
~
8 110 • 100 6 90
24
06
HOURS
Fig. 3. Diurnal variations of dissolved oxygen, pH, temperature and conductivity within the enclosure and of photosynthetic active radiation (PAR) and turbidity adjacent to the enclosure during different experiments. A: 23-25 N o v e m b e r 1985; B: 26-28 January 1986; C: 15-17 February 1986; D: 10-12 May 1986; E: 7-9 June 1986; F: 26-28 July 1986; G: 15-17 March 1988.
10
C. MACHENA ET AL.
piration values. For comparison, values from the different experiments are expressed as oxygen as well as carbon per unit dry weight of Lagarosiphon (Table 2 ). The net c o m m u n i t y production rate varied between - 4 . 9 and 4.86 mg C g-~ day-1 over the period with a mean value of 1.16 mg C g - l DW day -~. Given a mean standing biomass of Lagarosiphon of 100 g m - 2 between depths of 0 and 5 m (Machena and Kautsky, 1988 ) the net Lagarosiphon community production was 0.12 g C m - 2 day-~ or calculated for a year 42 g C m -2 year- ~, which is 6.5 times less than the value obtained using direct measurem e n t of changes in the weight of marked individual plants. Production:respiration ratios varied between 0.7 and 1.7 (Table 2). The ratio is lowest in February and increases to a m a x i m u m in July after which it begins to decline. Overall P : R ratios for the total c o m m u n i t y metabolism were 1.16, indicating a c o m m u n i t y close to a steady-state. DISCUSSION
The growth pattern of Lagarosiphon in Lake Kariba is similar to that of Potamogeton pectinatus in Lake Swartvlei (South Africa) (Howard-Williams, 1978 ). Both species have perennial populations with cohorts in different stages of development more or less during the whole year. M a x i m u m production of Potamogeton occurs in s u m m e r followed by a massive die-off of shoots and, like Lagarosiphon in Lake Kariba, growth and decay continue all year round. In Lake Kariba, the biomass ratio of senescent to young shoots is high (there are fewer young shoots than mature shoots) between February and October, so that even though the P: R ratio is high during other seasons, the production may be higher in summer. The mean production rate of Lagarosiphon derived from the enclosure experiments (over 7 months; Table 2 ) of 1.16 mg C g - ~ DW d a y - 1 is 6.5 times lower than the rate of 7.5 mg C g - 1 DW d a y - 1calculated from growth studies of marked plants. The large difference is due to the fact that the two techniques show different aspects of production, and the result from the enclosure experiments is a mean over different seasons. For example, the May production rate (Table 2 ) is fairly comparable with the rate derived from changes in plant length. However, the inclusion of results from both studies provides an enhanced understanding of c o m m u n i t y processes (cf. Kemp et al., 1986 ). In the enclosure experiments, net primary production is highly influenced by the total respiration of the community. In Lake Kariba, sediment respiration (measured by comparing respiration in a Lagarosiphon enclosure and in another enclosure covering bare sediment patches) is high, often accounting for as much as 42% of the respiration in enclosures (Machena, et al., 1989). This is probably one of the explanations for the lower net production rates found in the enclosure experiments.
LAGAROSIPHON ILICIFOLIUS IN LAKE KARIBA
11
However, from an ecosystem point of view, the measurement of community metabolism is attractive because it reflects the production of the entire system as well as its successional states. On the other hand, intermittent measurements of growth increments or harvesting give an integrated measure (over time) of the net production reflected as plant biomass. Growth increments or harvesting techniques though, will not take into account losses due to fragmentation and exudation. The large differences in the results from the two techniques could also be explained by the fact that the short-term measurements in the enclosures did not reflect the continuously changing environmental conditions in the open system. Light and turbidity changed continuously during incubation (Fig. 3 A - G ) . The enclosures were set up in shallow water and on a number of occasions, the wind blew offshore at night and onshore during the day. This caused turbidity during the day and limited light penetration. Hence, in view of these changing environmental conditions any extrapolation of short-term results to obtain production (yield) values for longer periods will thus present errors (Lipkin et al., 1986). On the other hand, measurement of growth gives the cumulative net production over an entire range of changing environmental conditions and therefore a more representative yield (Lipkin et al., 1986 ). The production rate of Lagarosiphon in Lake Kariba calculated to be 16.4 m g g -t DW day -1 or 7.5 mg C g-~ DW day -l (0.8 mg C g-1 DW h - l ) is rather low compared with literature data for other macrophyte species. Westlake( 1975 ) concluded that optimum production rates for a great variety of species are usually between 2 and 10 mg C g- 1 DW h - t and a mean value of 4 would be typical. However, the rates given by Westlake are maximum values; these are often taken under optimum light conditions and at the peak of the growing season and may not reflect a consistent rate of growth throughout the growing season, which should be lower than the maximum values. It should be pointed out that the hourly rate of growth, which we compare with Wesflake's, has been calculated assuming production over a 10-h period of daylight thereby underestimating our rate of Lagarosiphon production in Lake Kariba; if the maximum rate were calculated it may well fall within the range given by Westlake (1975). Also the photosynthetic rates of Lagarosiphon could be underestimated from the measurement in growth changes, as photosynthetic tissues represent only a portion of the whole plant, though the whole plant will be respiring. Our growth rate value of 16.4 mg g-~ DW day-1 for Lagarosiphon is also lower than the value of 25.7 mg g- ~ DW d a y - 1 for Potamogeton thunbergii Charm and Schlecht. calculated from the value of 0.18 g g-~ DW weekgiven in Denny (1985). Denny also gives a growth rate of 0.46 g g-~ DW week- ~ ( 65.7 mg g- 1DW d a y - ~) for P. schweinfurthii A. Bennett. The values given by Denny ( 1985 ) for P. thunbergii and P. schweinfurthii indicate high
12
c. MACHENAETAL.
rates of production consistent with the growth of tropical species. However, these plants were grown in ponds under ideal conditions. Furthermore the values incorporate changes in weight of shoots, rhizomes and roots. Contrary to this, growth changes of Lagarosiphon in Lake Kariba were followed in deeper water (depth varied from 3 to 4 m) and light could have been limiting as the maximum biomass of Lagarosiphon in Lake Kariba occurs between depths of 2 and 3 m (Machena and Kautsky, 1988). Measurements were started at a depth of 4 m to prevent exposure of the plants during the study following annual fluctuations in the lake level. At the end of the study depth was 3 m. Lake Kariba has a mean annual drawdown of 3 m. Total annual dry organic matter production of Lagarosiphon in Lake Kariba ranges from 12.8 to 861.3 g DW m - 2 year- ~ (mean of 492.8 g DW m - 2 ) , with a Lagarosiphon biomass in the lake ranging from 2.6 to 174.8 g DW m -2 (Machena and Kautsky, 1988). The within lake variability of macrophyte standing crop and production per unit area are about two orders of magnitude, which is similar to findings in other lakes (Carpenter and Lodge, 1986 ). The bio-energetics trend of the community is indicated by the month to month P : R ratios (Table 2). The P : R ratio for January is 1.09 and indicates a system close to steady-state. Maintenance metabolism is significant and equals the gross primary production. This ratio coincides with flowering and extensive branching of plants. In February the community progresses to heterotrophy with a P: R ratio of less than one. The excess of consumption over production is indicative of the declining state of the plants at this time of the year when there is a large scale die-off of shoots. The situation is reversed after May, when the system becomes autotrophic. The P: R ratios are similar to those recorded in other studies e.g. Hannan and Dorris (1970). Murray and Wetzel ( 1987 ) give an account of similar processes in the seagrass (Zostera marina L. and Ruppia martima L. ) communities in Chesapeake Bay, U.S.A. An annual summation of gross production and respiration of the Lagarosiphon community in this study gives an average ratio of 1.16. This indicates a high degree of self-maintenance throughout the whole study period. As the plants are the major producers of the community, this shows that a large proportion of the community production is stored in plant tissues that are not readily utilised by herbivores. This is consistent with our observation that there is little grazing on Lagarosiphon. All plants seemed to grow from fragmented shoots and we saw no evidence of plants developing from seeds although much flowering was observed between November and February (summer). Sexual reproduction does not seem to play an important role in the maintenance of many submerged macrophyte populations (Sculthorpe, 1967; Haag, 1983; Riemer, 1984; Kautsky, 1987), although seeds may be important to ensure survival in the event of disaster (van Wijk, 1983; Riemer, 1984). Mitchell ( 1969, 1970) also found that Sal-
LAGAROSIPHON ILICIFOLIUS 1N LAKE KARIBA
|3
vinia molesta D.S. Mitchell (a floating water fern) in Lake Kariba produces sterile spores and reproduces vegetatively. Length of Lagarosiphon varied from a few centimetres on unproductive sites to about 4 m in deep and sheltered areas of the lake (Machena, 1987 ). Not all plants flowered, branched and died in summer; cohorts which developed in summer, invested considerable energy in vegetative propagation. During the other seasons, little branching and flowering were evident though different cohorts are still going through a similar cycle. The community presents a dynamic flux comprising phases of building up, high maintenance and die-off. The steady-state is attained during the extensive branching period and progresses to heterotrophy at the massive die-off period. After the die-off there is increased light penetration through the water column that enhances growth of other cohorts leading to a positive energy balance, which is maintained for the remainder of the year. The die-off results in the formation of entangled floating mats of Lagarosiphon. At this stage the plant fragments have already started to develop roots, which enable a rapid establishment after contact with the substratum is made. These plant fragments either continue drifting, or sink and establish. In terrestrial communities vegetative propagation is efficacious for maintenance and new establishment around established plants (Grime, 1979). In the case of Lagarosiphon, vegetative propagation is important for colonisation of new areas and this might reduce the need for seeds. The average annual water fluctuation in the lake is about 3 m, and as the lake level rises following the summer rains, terrestrial vegetation is inundated. It has been observed that those plant fragments which drift to the shore with the current are trapped in the flooded vegetation and sink to the bottom where they establish new plants. By the time the flooded vegetation rots (34 months), a population of Lagarosiphon has already beett~stablished. The rapid annual growth, canopy formation at the water surface find the massive vegetative reproduction by stem fragments are competitive strategies (sensu Grime, 1979 and Kautsky, 1988 ), and these could account for the dominance of Lagarosiphon over other submerged macrophyte species in the lake (Machena, 1987). The big difference in the production values between the community taken as a whole and individual plants reflects the role other components of the ecosystem play in the metabolism of the macrophyte community. Sediment respiration in the Lagarosiphon community can be high (C. Machena et al., 1989 ) and this may overshadow the production of the plants in the community. For this reason the value of 16.4 mg DW g-1 day-1 could be a more realistic growth rate of Lagarosiphon.
14
c. MACHENAETAL.
ACKNOWLEDGEMENTS T h i s s t u d y w a s c a r r i e d o u t w i t h t h e s u p p o r t o f S A R E C , the S w e d i s h A g e n c y f o r R e s e a r c h C o o p e r a t i o n w i t h D e v e l o p i n g C o u n t r i e s . W e t h a n k P r o f e s s o r E. v a n d e r M a a r e l , P r o f e s s o r C. d e n H a r t o g , D r . C. S k a r p e , D r . A - M . J a n s s o n , D r . L. K a u t s k y a n d D r . J.F. T a l l i n g f o r t h e i r c o m m e n t s o n t h e m a n u s c r i p t . T. M o y o h e l p e d w i t h t h e diving. D. M w a i t a t y p e d t h e m a n u s c r i p t . M. v a n d e r M a a r e l - V e r s l u y s m a d e e d i t o r i a l checks. T h i s p a p e r is p u b l i s h e d w i t h t h e p e r m i s s i o n o f t h e D i r e c t o r o f N a t i o n a l P a r k s a n d W i l d Life M a n a g e m e n t , Zimbabwe.
REFERENCES Balon, E.K. and Coche, A.G., 1974. Late Kariba: A Man-made Tropical Ecosystem in Central Africa. Junk, The Hague. Carpenter, S.R. and Lodge, D.M., 1986. Effects of submerged macrophytes on ecosystem processes. Aquat. Bot., 26". 341-370. Cattaneo, A. and Kalff, J., 1980. The relative contribution of aquatic macrophytes to the production of macrophyte beds. Limnol. Oceanogr., 25: 280-289. Coche, A.G., 1968. Description of the physico-chemical aspects of Lake Kariba, an impoundment in Zambia-Rhodesia. Fish. Res. Bull. Zambia, 5: 200-267. Davies, G.S., 1970. Productivity of macrophytes in Marion Lake, British Columbia. J. Fish. Res. Board Can., 27: 71-78. Denny, P., 1985. The structure and functioning of African euhydrophyte communities. The floating-leaved and submerged vegetation. In: P. Denny (Editor). The Ecology and Management of African Wetland Vegetation. Junk, The Hague, pp. 125-151. Dybern, B.I., Ackerfors, H. and Elmgren, R. (Editors), 1976. Recommendations on methods for biological studies in the Baltic Sea. Baltic Mar. Biol., l: 1-98. Grime, J.P., 1979. Plant Strategies and Vegetation Processes. Wiley, Chichester, 222 pp. Haag, R.W., 1983. Emergence of seedlings of aquatic macrophytes from lake sediments. Can. J. Bot., 61: 148-156. Hannan, H.H. and Dorris, T.C., 1970. Succession of macrophyte community in a constant temperature river. Limnol. Oceanogr., 15: 442-453. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London. Howard-Williams, C., 1978. Growth and production of aquatic macrophytes in a south temperature saline lake. Verb. Int. Verein. Limnol., 20:1153-1158. Howard-Williams, C. and Allanson, B.R., 1981. An integrated study on littoral and pelagic primary production in a Southern African coastal lake. Arch. Hydrobiol., 92: 507- 534. Hunt, R., 1978. Plant Growth Analysis: Studies in Biology, no. 96. E. Arnold, London, 67 pp. Jansson, B.O. and Wulff, F., 1977. Ecosystem analysis of a shallow sound in the northern Baltic - a joint study by the Ask/5 group. Contrib. Askti Lab. Univ. Stockholm, 18: l-160. Kautsky, L., 1987. Life cycles of three populations of Potamogeton pectinatus L. at different degrees of wave exposure in the Aski3 Area, Northern Baltic proper. Aquat. Bot., 27:177186. Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos, 53:126-135. Kemp, W.M., Lewis, M.R. and Jones, T.W., 1986. Comparison of methods for measuring pri-
LAGAROSIPHON IL1CIFOLIUS IN LAKE KARIBA
15
mary production by the submerged macrophyte Potamogeton perfoliatus L. Limnol. Oceanogr., 31: 1322-1334. Lrv~que, C., Dejoux, C. and Lauzanne, L., 1983. Lake Chad, ecology and productivity of a shallow tropical ecosystem. J.P. Carmouze, J.R. Durand and C. Lrv~que (Editors). Junk, The Hague. Lipkin, Y., Beer, S. Best, E.P.H., Kairesalo, T. and Salonen, K., 1986. Primary production of macrophytes: terminology, approaches and a comparison of methods. Aquat. Bot., 26: 129142. Machena, C., 1987. Zonation of submerged macrophyte vegetation and its ecological interpretation in Lake Kariba. Vegetatio, 73:111-119. Machena, C. and Kautsky, N., 1988. A quantitative diving survey of benthic vegetation and fauna in Lake Kariba - a tropical man-made lake. Freshwater Biol., 19: 1-14. Machena, C., Kautsky, N. and Lindmark, G , 1989. Metabolism and nutrient dynamics in Lagarosiphon ilicifolius in tropical Lake Kariba. In: Ecology of the Hydrolittoral Macrophyte Communities in Lake Kariba, Ph.D. Thesis, University of Uppsala. McLachlan, A.J. and McLachlan, S.M., 1971. Benthic fauna and sediments in the newly created Lake Kariba (Central Africa). Ecology, 52: 800-809. Mitchell, D.S., 1969. The ecology of vascular hydrophytes on Lake Kariba. Hydrobiologia, 34: 448-460. Mitchell, D.S., 1970. Autecological studies of Salvinia aurticulata Aubl. Ph.D. thesis. University of London. Morgan, M.D. and Kitting, C.L., 1984. Productivity and utilization of the seagrass Halodule wrightii and its attached epiphytes. Limnol. Oceanogr., 29:1066-1076. Murray, L. and Wetzel, R.L., 1987. Oxygen production and consumption associated with the major autotrophic components in two temperate sea grass communities. Mar. Ecol. Progr. Set., 38: 231-239. Pelican, J. Hudec, K. and Stastny, K., 1978. Animal populations in fish pond littorals. In: D.D. Dykyjov~t and J. Kv~t (Editors), Ecological Studies 28 Pond Littoral Ecosystems. Structure and Function. Springer, pp. 74-79. Rich, P.H., Wetzel, R.G. and Van Thuy, N., 1971. Distribution, production and role of aquatic macrophytes in a southern Michigan marl lake. Freshwater Biol., 1: 3-21. Riemer, D.N., 1984. Introduction of Freshwater Vegetation. AVI Publishing Co., Westport, CT. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular plants. E. Arnold, London, 610 pp. Solander, C.D., 1982. Production of macrophytes in two small, sub-arctic lakes in northern Sweden. In: J.J. Symoens, S.S. Hooper and P. Compare (Editors), Studies of Aquatic Vascular Plants. Royal Botanical Society of Belgium, pp. 181-186. Van Wijk, R.T., 1983. Life cycles and reproductive strategies of Potamogeton pectinatus L. in the Netherlands and the Camargue (France). Proceedings International Symposium of Aquatic Macrophytes, Nijmegen, 18-23 September, 1983. Voilenweider, R.A., 1974. A Manual on Methods for Measuring Primary Production in Aquatic Environment. IBM Handbook, no. 12. Blackwell, London, 213 pp. Westlake, D.F., 1975. Primary production of freshwater macrophytes. In: J.P. Cooper (Editor), Photosynthesis and Productivity in Different Environments. Cambridge University Press, pp. 189-206. Wetzel, R.G. and Hough, R.A., 1973. Productivity and role of aquatic macrophytes in lakes. An assessment. Pol. Arch. Hydrobiol., 20: 9-19.
1
Elsevier Science Publishers B.V., A m s t e r d a m - - P r i n t e d in T h e N e t h e r l a n d s
Growth and production of Lagarosiphon ilicifolius in Lake Kariba a man-made tropical lake
C e c i l M a c h e n a 1, N i l s K a u t s k y 2 a n d G u n i l l a L i n d m a r k 3
~Lake Kariba Fisheries Research Institute, P.O. Box 75, Kariba, Zimbabwe and lnstitute of Ecological Botany, Uppsala University, P.O. Box 559, S-751 22 Uppsala (Sweden) 2Ask~ Laboratory, Institute of Marine Ecology and Department of Zoology, University Stockholm, S-106 91, Stockholm (Sweden) 31nstitute of Limnology, University of Lund, Box 65, S-221 00, Lund (Sweden) (Accepted for publication 31 October 1989)
ABSTRACT Machena, C., Kautsky, N. and Lindmark, G., 1990. Growth and production ofLagarosiphon ilicifolius in Lake Kariba - - a man-made tropical lake. Aquat. Bot., 37:1-15.
Two different methods, the diurnal oxygen curve method in plexiglass enclosures, and the incremental growth technique were used to complement production estimations ofLagarosiphon ilicifolius Oberm. in Lake Kariba. The incremental growth technique gave a production rate of 16.4 mg g - ~dry weight ( D W ) d a y - ~ (7.5 mg C g - ~ DW d a y - t ) which was 6.5 times higher than the rate of 1.16 mg C g - ~ DW d a y - ~obtained for the community from the diurnal oxygen curve method. The difference is largely accounted for by the total respiration of the community, which is inherent to the enclosure technique, and also by the fact that the measurements were carried out for short periods of time. Using the production rate from growth measurements, the biomass production of Lagarosiphon was calculated as 1.6 g DW m -2 d a y - ~and to 598.6 g m -2 year- 1. The average community P / R ratio of 1.16 indicates that the community is operating close to steadystate, and shows a high degree of self maintenance. Lagarosiphon has an annual turnover rate of 2.4 but the populations are perennial (i.e. grow all year round). The main growing season is in summer, from October to February. Cohorts that develop during the summer, branch extensively at the end of this growth period, and while occluding light to the bottom, die off in the process. The resulting drifting mats fragment and constitute the major reproductive modules. Although flowering was observed, sexual reproduction does not appear to be important. It is concluded that the difference in the production values between the community taken as a whole and individual plants reflects the role different components of the ecosystem play in the metabolism of the macrophyte community. For this reason the value of 16.4 mg g-~ day-~ calculated from marked individuals is a more realistic growth rate of Lagarosiphon plants in this study.
0304-3770/90/$03.50
© 1990 Elsevier Science Publishers B.V.
2
C. MACHENA ET AL.
INTRODUCTION
This study was carried out to estimate the productivity of a Lagarosiphon ilicifolius Oberm. dominated c o m m u n i t y and to follow the growth and phenology of Lagarosiphon in Lake Kariba. A number of standard methods for primary production measurements have been r e c o m m e n d e d (Vollenweider, 1974; Kemp et al., 1986). In the present study we use two of them: changes in growth over time in marked plants, and in situ studies of oxygen production and its seasonal variation in plexiglass enclosures. Benthic macrophytes (i.e. macrophytes living on the bottom of the lake) form productive communities (Cattaneo and Kalff, 1980; Morgan and Kitting, 1984) and are important for fisheries. Their contribution to the total biomass production is generally related to the size and morphometry of the water body. For some shallow lakes e.g. Swartvlei (Howard-Williams, 1978 ) and Lake Chad (L6v6que et al., 1983 ) hydrolittoral (i.e. the zone extending from the water-line to the depth at which plants are rooted) production exceeds pelagic planktonic algal production. However, for deeper lakes the opposite usually holds. Benthic macrophytes are also important in the lake as a substrate for microand macrofauna and epiphytic algae (McLachlan and McLachlan, 1971; Wetzel & Hough, 1973; Pelican et al., 1978; Howard-Williams and Allanson, 1981; Morgan & Kitting, 1984; Carpenter and Lodge, 1986). Machena and Kautsky ( 1988 ) argued that the development of the submerged vegetation in Lake Kariba facilitated the development of other benthic communities, particularly gastropods and bivalves. As Lagarosiphon is the dominant species regarding both biomass (Machena and Kautsky, 1988) and area covered (Machena, 1987), production studies on this species may give an indication of the role of macrophytes in the ecology of the lake. MATERIAL AND METHODS
Study area Lake Kariba (16028 ' to 18°06'S; 26004 ' to 2 9 ° 0 3 ' E ) is an artificial lake formed after d a m m i n g of the Zambezi River. It is located in Southern Africa between Zambia and Zimbabwe and is the third largest man-made lake in the world. Its features and morphology are presented in Table 1. The main axis of the lake has a SW-NE orientation following the old Zambezi River basin. (For details see Balon and Coche, 1974). Two sites were chosen, one close to the Fisheries Research Institute at the eastern end of the lake where c o m m u n i t y metabolism studies were carried out
LAGA I~OSIPHON ILICIFOLIUS IN LAKE KARIBA
3
TABLE 1 Main features and morphology of Lake Kariba at a water level of 485 m a.s.1. Partly recalculated from Balon and Coche (1974), and potential colonisable areas of submerged macrophytes Length Width (mean) Depth (mean) Depth (maximum) Area Average bottom area per 1 m depth interval between 0-15 m Total bottom area between 0 and 5 m deep Volume Percentage of bottom area between 0 and 15 m deep Total length of shoreline
277.0 19.4 29.2 120.0 5364.0
km km m m km 2
105.2 km 2 m 526.1 km z 156× 109 m 3 23.5% 2668.0 km
and the other half-way along the Zimbabwean side of the lake where the growth of individual plants was followed. Site 1 is on an exposed shore, which is regularly subjected to turbidity from wave action. Studies at the site were carried out at a depth of 1 m. Site 2 was situated 4 m deep and about 1 km offshore. The standing crop of Lagarosiphon was similar at both sites and also similar to the mean standing crop for the lake within the colonised zone between depths of 0 and 5 m (Machena and Kautsky, 1988).
Measurement of growth rates Growth rate was measured on individually marked Lagarosiphon ilicifolius plants that had grown from fragmented shoots. In October when the plants were small (unbranched with an average length of 20 _+2.65 cm), a total of 40 plants in 4 (0.5×0.5 m ) quadrats were individually marked. Pieces of steel rods were pushed into the ground alongside each identified ramet (Harper, 1977) to distinguish these from plants that would establish later during the study. The positions of the plants in each quadrat were then marked on roughened plastic sheets (for use under water) on which all data were recorded. The marked plants were assumed to be of the same age and are treated as one cohort. The total length of each shoot and its branches were measured in cm once every m o n t h from October 1986 until the plants senesced in April 1987. Lagarosiphon is rooted and grows vertically with little branching until it reaches close to the water surface where it branches extensively thereby in-
4
C. MACHENA ET AL.
creasing its photoreceptive surface area. A length:weight regression was calculated using plants collected from the same population as the marked plants Y= 3 . 0 4 X - 5.5
( n = 36; r2=0.96)
(1)
where Y= dry weight (mg) and X = total length of shoot and branches (cm). This equation was used to calculate the weight increments for each month. Relative growth rates were calculated using Eqn. (2) as outlined in Hunt (1978) R-
log~ W2- log~ Wl
T2- T,
(2)
where W1 is dry weight in g at time T1 in days and W2 is dry weight at time T2 and e is the base of the natural logarithm. The mineral ash (inorganic) content of the plants, which amounted to 17.5%, (as measured once in the early part of the study) was subtracted from the weight increments. This provided values for changes in the organic weight (Hunt, 1978) expressed per unit dry weight of the plant biomass and was found to be similar to the value of 15% reported for Ceratophyllum demersum L. by Lipkin et al. (1986). Areal photosynthetic rates were calculated using Eqn. (3):
Pr=CO mgg -1 day-1 × B
(3)
where Pr= areal production; C = changes in organic weight per unit weight of plant per unit time (rag g-~ day -1 ); B=biomass (g DW m -2) of Lagarosiphon. Changes in weight in this paper refer to organic weight. The carbon content of Lagarosiphon was assumed to be 46% of the total organic weight (ash-free DW) (Davies, 1970; Westlake, 1965 in Solander, 1982); the ash content was determined by ignition in a muffle oven at 550°C. Denny ( 1985 ) gives the carbon contents of leaf tissues ofPotamogeton pectinatus L. between 42 and 49%. Annual variation in the carbon content of the plants was assumed to be insignificant (Solander, 1982 ).
Measurement of community metabolism Oxygen production and consumption The community metabolism of Lagarosiphon was calculated using diurnal oxygen curves as described in Jansson and Wulff ( 1977 ) (see also Dybern et al., 1976 ). The communities were enclosed in plexiglass cylinders in situ with a lid on top, which enclosed a surface area of 0.066 m z and a water volume of 22.4 1. The lid had two outlets, one for withdrawing water samples and the other one for inserting the oxygen probe. The cylinder was pushed gently into the substrate to ensure a substrate seal and was held in position by four steel bars to prevent tipping of the cylinder from wave action.
5.9 7.3 9.0 2.9 3.8 8.7 8.7
cylinder (g DW)
Lag. in
19.93 30.9 31.7 29.6 24.75 22.9 9.48
(7.49) (11.6) (11.9) (11.13) (9.30) (8.61) (3.56)
Gross production ~ (GP: mg 02 g- ~day- ~)
1.78 (0.67) 3.4 (1.3) 4.31(1.6) 1.30(0.49) 1.19 (0.44) 3.02 (1.11) 1.24 (0.47)
Areal 2 Gross production (A/~. g 02 m -2 day- t ) 1.55 3.1 6.1 1.8 0.96 1.7 1.33
(0.58) (1.2) (2.3) (0.41) (0.37) (0.6) (0.50)
Areal 2 community respiration (AR:gO2m-2day -l) 0.98 0.9 -4.9 4.86 3.1 3.6 -0.24
Net community production (PN:mgCg-lday -l)
17.31 28.4 44.9 16.66 16.68 13.09 10.12
(6.51) 1.15 (10.7) 1.09 (16.8)0.71 (6.27) 1.20 (6.2) 1.24 (4.92) 1.77 (3.80) 0.93
Community respiration AP/AR (CR:mgO2g-lday -t)
tProduction or respiration values per unit weight of plant obtained by dividing changes in oxygen levels in the enclosure by the weight of plant harvested in the enclosure. 2Areal values of production and respiration obtained by extrapolating total values within the enclosure to m 2. 3Refers to Fig. 3; Lag. =L. ilicifolius.
A23-25/I1/85 B26-28/01/86 C15-17/02/86 D10-12/05/86 E 07-09/06/86 F26-28/07/86 G 15-17/03/88
Period of study 3
Lagarosiphon ilicifolius community metabolism in plexiglass enclosures. Carbon equivalents of production and respiration values are given in parentheses
TABLE 2
:m
t'rl
7~
6
C. MACHENA ET AL.
Diurnal measurements were begun at dusk and continued for about 37 h, thus covering a full day and the nights before and after. A battery powered bilge p u m p stirred water within the cylinder either continuously or at intervals. Dissolved oxygen and temperature readings were taken every hour using a Yellow Springs 58 oxygen meter with a combined oxygen and temperature probe. At the end of each experiment (carried out during the periods indicated in Table 2 ), the enclosed plants and animals were collected, separated by species and dried to constant weight. Oxygen production and consumption were calculated from diurnal oxygen mass time curves. The respiration rate was calculated as the best fitting slope on night consumption. This was extrapolated to 24 h to obtain total daily respiration. When the best fitting slope on night consumption was continued, the height between this slope and the mass time curve after 24 h of incubation, gave daily gross oxygen production. C o m m u n i t y production and consumption rates were calculated on a unit area basis. As Lagarosiphon was the dominant producer, production and consumption rates were also calculated on a Lagarosiphon unit weight basis.
pH, conductivity, turbidity and light measurement The physical parameters pH, conductivity, turbidity and photosynthetic active radiation (PAR), were measured in the enclosure to help elucidate biological and physical processes in the enclosures. Water samples were taken from the lake m e d i u m and siphoned from the experimental cylinders every 3 h and pH, conductivity and turbidity were measured immediately. Conductivity was determined with a portable Crison meter (model 523) and pH was measured with a Crison portable pH meter 506 and a combined pH electrode. Turbidity was measured as N T U (normal turbidity units ) with a Hach model 16 800 portable turbidimeter. Light penetration (photosynthetic active radiation PAR, 400-700 n m ) adjacent to and at about the centre of the cylinders was measured with a LI-COR- 188B integrating q u a n t u m sensor (submersible) and meter. Total daily PAR was derived by planimetric integration of hourly PAR values. RESULTS
Growth measurement The growth curve (DW) and phenology of individual shoots of Lagarosiphon are shown in Figs. 1 and 2. The plant weight increased rapidly from a mean of 61.6 mg per shoot in October to a mean of 225 mg per shoot in February, when the shoots matured. The production rate was consistently high between October and January when flowering and rapid branching occurred. By February the shoots were
7
LAGAROSIPHON ILICIFOLIUS IN LAKE K A R I B A
300-
-]00 DEATH
1
250~200-
FLOWERING/
?,
u}
60
BRANCHING|/
150-
100-
20
50-
l
ASO
l
i
N
,
i
DJ
i
r
t
,
F M A M J
Fig. 1. Growth of Lagarosiphon ilicifolius L. in Lake Kariba. The onset of branching and death is indicated. Vertical bars are SE of means.
BRANCHING AND FLOWERING
DRIFTING FRAGMENTS
WATER SURFACE 120'
I--r ~" 100' z k0 o -r 80 u~ 60
4020-
( O
N
F
M
Fig. 2. A diagrammatic representation of the growth cycle of Lagarosiphon Kariba showing a marked density of mature shoots at the water surface.
ilic(folius in Lake
8
C. MACHENA ET AL.
extensively branched and attained a m a x i m u m length of 160 cm. Senescence began in February, as evidenced by shoots rotting from the substratum, and by April all plants were detached or dead. As the marked shoots were assumed to be of the same age, the growth period of the cohort can be estimated at 5 months. As the Lagarosiphon populations are perennial in Lake Kariba, this gives a turnover of 2.4 for overall annual net production. Rich et al. ( 1971 ) reported an annual turnover of 1.5 and 3.0, using two different techniques for macrophytes in a Michigan marl lake, and projected a possible range of 0.5 to 5 for macrophytes in general. The mean net production rate for measurement of individual shoots was 16.4 mg g-~ DW day-1. By dividing the daily production rate by l0 (hours of day- light), the hourly value of 1.7 mg g-1 DW was obtained. In terms of net carbon production this is equivalent to 7.5 mg C g-~ DW day-1. Calculations of areal production rate were made using a mean biomass of Lagarosiphon of 100 g m -2 (for the colonised zone of 0-5 m water depth given in Machena and Kautsky ( 1988 ). A mean areal production rate of 1.6 X 103 mg DW m -2 day -1, equivalent to 754 mg C m -2 day -1 was obtained.
Community metabolism The in situ enclosure experiments were performed during different seasons (Table 2 ) to cover variation in environmental conditions and development phases of Lagarosiphon (Fig. 3 ). The diurnal changes in pH, PAR, turbidity, temperature, conductivity and dissolved oxygen are presented in Fig. 3 A-G. As expected, values for temperature, pH and oxygen were lowest in the early morning and peaked late in the afternoon, reflecting normal physical and biological activity. The pH varied by 0.5-1.3 units during 24 h and the total pH span was 6.7-9.5. The increase in pH during photosynthesis is due to the utilisation of carbon dioxide in the production process. The diurnal amplitude for water temperature was 2 °-4 °C and the total temperature range covered by the experiments was 22 °33°C. Conductivity values ranged between 109 and 145/t S c m - 1 during the day. The changes in conductivity are more complex and less consistent, as several interlinked factors and c o m m u n i t y components are involved in the mineralisation process. PAR varied irregularly and was inversely related to turbidity (Fig. 3 ). However, the low PAR values in the early part of the incubation obtained in March ! 988 were due to the light sensor being shaded by vegetation. From variations in the oxygen production and consumption in the enclosure experiments, values for gross production and c o m m u n i t y respiration have been estimated (Table 2). The variation in the weight of the plants in different enclosures was considered when calculating the production and res-
9
LAGAROSIPHON ILICIFOLIUS Ie LAKEKARIBA T C
o:
p} ,'CONDUC-
6 30
~-..~
i~//~__~...~
4 28
~
"
~z ~ ~-,
2 26
" 120
160.20 801 I0
A
1oo
8 F29 6 r28 4 27
110
'20
2 26
,10
6
~-.........
Ft 8
30
100
/---\
6 29
- - __
i150 140
\/
4 28
20
2 27
'10
f
130
112° /
C
.
.
.
9. 29
"Jl
8.28
.-~jr-~i
.
.
.
71110
./,~'~ ~ \
120 ~
~
110
6' 27
8 100 20
4" 2 6
90
10 ,:'
,
.
7 80
10" 27 8" 26
130
6 25 4 24
i 20 - - ' - - -
2 23 E
-
....
~C~
--
10
.,:,~', ~: , c . ,
12 26 10 25
~
8-24
.
8 120 "110 "100 , 7 "90
12 130 11 120
/
6.23
10 110 9 100
4 "22 2.21
F TEN"~RATURE
pH
---- CONDUCTIVITY
PAR
TURBIDITY
I
~. . . .
__ 6.2e
120 10
. " : ! ,: ?~,.,
~
"""~'--.~'~""
427
~
------...
----~
/~
: : :
226
20 0
.<;i:...
G i
18
24
06
12
18
8 90
7 80
~
8 110 • 100 6 90
24
06
HOURS
Fig. 3. Diurnal variations of dissolved oxygen, pH, temperature and conductivity within the enclosure and of photosynthetic active radiation (PAR) and turbidity adjacent to the enclosure during different experiments. A: 23-25 N o v e m b e r 1985; B: 26-28 January 1986; C: 15-17 February 1986; D: 10-12 May 1986; E: 7-9 June 1986; F: 26-28 July 1986; G: 15-17 March 1988.
10
C. MACHENA ET AL.
piration values. For comparison, values from the different experiments are expressed as oxygen as well as carbon per unit dry weight of Lagarosiphon (Table 2 ). The net c o m m u n i t y production rate varied between - 4 . 9 and 4.86 mg C g-~ day-1 over the period with a mean value of 1.16 mg C g - l DW day -~. Given a mean standing biomass of Lagarosiphon of 100 g m - 2 between depths of 0 and 5 m (Machena and Kautsky, 1988 ) the net Lagarosiphon community production was 0.12 g C m - 2 day-~ or calculated for a year 42 g C m -2 year- ~, which is 6.5 times less than the value obtained using direct measurem e n t of changes in the weight of marked individual plants. Production:respiration ratios varied between 0.7 and 1.7 (Table 2). The ratio is lowest in February and increases to a m a x i m u m in July after which it begins to decline. Overall P : R ratios for the total c o m m u n i t y metabolism were 1.16, indicating a c o m m u n i t y close to a steady-state. DISCUSSION
The growth pattern of Lagarosiphon in Lake Kariba is similar to that of Potamogeton pectinatus in Lake Swartvlei (South Africa) (Howard-Williams, 1978 ). Both species have perennial populations with cohorts in different stages of development more or less during the whole year. M a x i m u m production of Potamogeton occurs in s u m m e r followed by a massive die-off of shoots and, like Lagarosiphon in Lake Kariba, growth and decay continue all year round. In Lake Kariba, the biomass ratio of senescent to young shoots is high (there are fewer young shoots than mature shoots) between February and October, so that even though the P: R ratio is high during other seasons, the production may be higher in summer. The mean production rate of Lagarosiphon derived from the enclosure experiments (over 7 months; Table 2 ) of 1.16 mg C g - ~ DW d a y - 1 is 6.5 times lower than the rate of 7.5 mg C g - 1 DW d a y - 1calculated from growth studies of marked plants. The large difference is due to the fact that the two techniques show different aspects of production, and the result from the enclosure experiments is a mean over different seasons. For example, the May production rate (Table 2 ) is fairly comparable with the rate derived from changes in plant length. However, the inclusion of results from both studies provides an enhanced understanding of c o m m u n i t y processes (cf. Kemp et al., 1986 ). In the enclosure experiments, net primary production is highly influenced by the total respiration of the community. In Lake Kariba, sediment respiration (measured by comparing respiration in a Lagarosiphon enclosure and in another enclosure covering bare sediment patches) is high, often accounting for as much as 42% of the respiration in enclosures (Machena, et al., 1989). This is probably one of the explanations for the lower net production rates found in the enclosure experiments.
LAGAROSIPHON ILICIFOLIUS IN LAKE KARIBA
11
However, from an ecosystem point of view, the measurement of community metabolism is attractive because it reflects the production of the entire system as well as its successional states. On the other hand, intermittent measurements of growth increments or harvesting give an integrated measure (over time) of the net production reflected as plant biomass. Growth increments or harvesting techniques though, will not take into account losses due to fragmentation and exudation. The large differences in the results from the two techniques could also be explained by the fact that the short-term measurements in the enclosures did not reflect the continuously changing environmental conditions in the open system. Light and turbidity changed continuously during incubation (Fig. 3 A - G ) . The enclosures were set up in shallow water and on a number of occasions, the wind blew offshore at night and onshore during the day. This caused turbidity during the day and limited light penetration. Hence, in view of these changing environmental conditions any extrapolation of short-term results to obtain production (yield) values for longer periods will thus present errors (Lipkin et al., 1986). On the other hand, measurement of growth gives the cumulative net production over an entire range of changing environmental conditions and therefore a more representative yield (Lipkin et al., 1986 ). The production rate of Lagarosiphon in Lake Kariba calculated to be 16.4 m g g -t DW day -1 or 7.5 mg C g-~ DW day -l (0.8 mg C g-1 DW h - l ) is rather low compared with literature data for other macrophyte species. Westlake( 1975 ) concluded that optimum production rates for a great variety of species are usually between 2 and 10 mg C g- 1 DW h - t and a mean value of 4 would be typical. However, the rates given by Westlake are maximum values; these are often taken under optimum light conditions and at the peak of the growing season and may not reflect a consistent rate of growth throughout the growing season, which should be lower than the maximum values. It should be pointed out that the hourly rate of growth, which we compare with Wesflake's, has been calculated assuming production over a 10-h period of daylight thereby underestimating our rate of Lagarosiphon production in Lake Kariba; if the maximum rate were calculated it may well fall within the range given by Westlake (1975). Also the photosynthetic rates of Lagarosiphon could be underestimated from the measurement in growth changes, as photosynthetic tissues represent only a portion of the whole plant, though the whole plant will be respiring. Our growth rate value of 16.4 mg g-~ DW day-1 for Lagarosiphon is also lower than the value of 25.7 mg g- ~ DW d a y - 1 for Potamogeton thunbergii Charm and Schlecht. calculated from the value of 0.18 g g-~ DW weekgiven in Denny (1985). Denny also gives a growth rate of 0.46 g g-~ DW week- ~ ( 65.7 mg g- 1DW d a y - ~) for P. schweinfurthii A. Bennett. The values given by Denny ( 1985 ) for P. thunbergii and P. schweinfurthii indicate high
12
c. MACHENAETAL.
rates of production consistent with the growth of tropical species. However, these plants were grown in ponds under ideal conditions. Furthermore the values incorporate changes in weight of shoots, rhizomes and roots. Contrary to this, growth changes of Lagarosiphon in Lake Kariba were followed in deeper water (depth varied from 3 to 4 m) and light could have been limiting as the maximum biomass of Lagarosiphon in Lake Kariba occurs between depths of 2 and 3 m (Machena and Kautsky, 1988). Measurements were started at a depth of 4 m to prevent exposure of the plants during the study following annual fluctuations in the lake level. At the end of the study depth was 3 m. Lake Kariba has a mean annual drawdown of 3 m. Total annual dry organic matter production of Lagarosiphon in Lake Kariba ranges from 12.8 to 861.3 g DW m - 2 year- ~ (mean of 492.8 g DW m - 2 ) , with a Lagarosiphon biomass in the lake ranging from 2.6 to 174.8 g DW m -2 (Machena and Kautsky, 1988). The within lake variability of macrophyte standing crop and production per unit area are about two orders of magnitude, which is similar to findings in other lakes (Carpenter and Lodge, 1986 ). The bio-energetics trend of the community is indicated by the month to month P : R ratios (Table 2). The P : R ratio for January is 1.09 and indicates a system close to steady-state. Maintenance metabolism is significant and equals the gross primary production. This ratio coincides with flowering and extensive branching of plants. In February the community progresses to heterotrophy with a P: R ratio of less than one. The excess of consumption over production is indicative of the declining state of the plants at this time of the year when there is a large scale die-off of shoots. The situation is reversed after May, when the system becomes autotrophic. The P: R ratios are similar to those recorded in other studies e.g. Hannan and Dorris (1970). Murray and Wetzel ( 1987 ) give an account of similar processes in the seagrass (Zostera marina L. and Ruppia martima L. ) communities in Chesapeake Bay, U.S.A. An annual summation of gross production and respiration of the Lagarosiphon community in this study gives an average ratio of 1.16. This indicates a high degree of self-maintenance throughout the whole study period. As the plants are the major producers of the community, this shows that a large proportion of the community production is stored in plant tissues that are not readily utilised by herbivores. This is consistent with our observation that there is little grazing on Lagarosiphon. All plants seemed to grow from fragmented shoots and we saw no evidence of plants developing from seeds although much flowering was observed between November and February (summer). Sexual reproduction does not seem to play an important role in the maintenance of many submerged macrophyte populations (Sculthorpe, 1967; Haag, 1983; Riemer, 1984; Kautsky, 1987), although seeds may be important to ensure survival in the event of disaster (van Wijk, 1983; Riemer, 1984). Mitchell ( 1969, 1970) also found that Sal-
LAGAROSIPHON ILICIFOLIUS 1N LAKE KARIBA
|3
vinia molesta D.S. Mitchell (a floating water fern) in Lake Kariba produces sterile spores and reproduces vegetatively. Length of Lagarosiphon varied from a few centimetres on unproductive sites to about 4 m in deep and sheltered areas of the lake (Machena, 1987 ). Not all plants flowered, branched and died in summer; cohorts which developed in summer, invested considerable energy in vegetative propagation. During the other seasons, little branching and flowering were evident though different cohorts are still going through a similar cycle. The community presents a dynamic flux comprising phases of building up, high maintenance and die-off. The steady-state is attained during the extensive branching period and progresses to heterotrophy at the massive die-off period. After the die-off there is increased light penetration through the water column that enhances growth of other cohorts leading to a positive energy balance, which is maintained for the remainder of the year. The die-off results in the formation of entangled floating mats of Lagarosiphon. At this stage the plant fragments have already started to develop roots, which enable a rapid establishment after contact with the substratum is made. These plant fragments either continue drifting, or sink and establish. In terrestrial communities vegetative propagation is efficacious for maintenance and new establishment around established plants (Grime, 1979). In the case of Lagarosiphon, vegetative propagation is important for colonisation of new areas and this might reduce the need for seeds. The average annual water fluctuation in the lake is about 3 m, and as the lake level rises following the summer rains, terrestrial vegetation is inundated. It has been observed that those plant fragments which drift to the shore with the current are trapped in the flooded vegetation and sink to the bottom where they establish new plants. By the time the flooded vegetation rots (34 months), a population of Lagarosiphon has already beett~stablished. The rapid annual growth, canopy formation at the water surface find the massive vegetative reproduction by stem fragments are competitive strategies (sensu Grime, 1979 and Kautsky, 1988 ), and these could account for the dominance of Lagarosiphon over other submerged macrophyte species in the lake (Machena, 1987). The big difference in the production values between the community taken as a whole and individual plants reflects the role other components of the ecosystem play in the metabolism of the macrophyte community. Sediment respiration in the Lagarosiphon community can be high (C. Machena et al., 1989 ) and this may overshadow the production of the plants in the community. For this reason the value of 16.4 mg DW g-1 day-1 could be a more realistic growth rate of Lagarosiphon.
14
c. MACHENAETAL.
ACKNOWLEDGEMENTS T h i s s t u d y w a s c a r r i e d o u t w i t h t h e s u p p o r t o f S A R E C , the S w e d i s h A g e n c y f o r R e s e a r c h C o o p e r a t i o n w i t h D e v e l o p i n g C o u n t r i e s . W e t h a n k P r o f e s s o r E. v a n d e r M a a r e l , P r o f e s s o r C. d e n H a r t o g , D r . C. S k a r p e , D r . A - M . J a n s s o n , D r . L. K a u t s k y a n d D r . J.F. T a l l i n g f o r t h e i r c o m m e n t s o n t h e m a n u s c r i p t . T. M o y o h e l p e d w i t h t h e diving. D. M w a i t a t y p e d t h e m a n u s c r i p t . M. v a n d e r M a a r e l - V e r s l u y s m a d e e d i t o r i a l checks. T h i s p a p e r is p u b l i s h e d w i t h t h e p e r m i s s i o n o f t h e D i r e c t o r o f N a t i o n a l P a r k s a n d W i l d Life M a n a g e m e n t , Zimbabwe.
REFERENCES Balon, E.K. and Coche, A.G., 1974. Late Kariba: A Man-made Tropical Ecosystem in Central Africa. Junk, The Hague. Carpenter, S.R. and Lodge, D.M., 1986. Effects of submerged macrophytes on ecosystem processes. Aquat. Bot., 26". 341-370. Cattaneo, A. and Kalff, J., 1980. The relative contribution of aquatic macrophytes to the production of macrophyte beds. Limnol. Oceanogr., 25: 280-289. Coche, A.G., 1968. Description of the physico-chemical aspects of Lake Kariba, an impoundment in Zambia-Rhodesia. Fish. Res. Bull. Zambia, 5: 200-267. Davies, G.S., 1970. Productivity of macrophytes in Marion Lake, British Columbia. J. Fish. Res. Board Can., 27: 71-78. Denny, P., 1985. The structure and functioning of African euhydrophyte communities. The floating-leaved and submerged vegetation. In: P. Denny (Editor). The Ecology and Management of African Wetland Vegetation. Junk, The Hague, pp. 125-151. Dybern, B.I., Ackerfors, H. and Elmgren, R. (Editors), 1976. Recommendations on methods for biological studies in the Baltic Sea. Baltic Mar. Biol., l: 1-98. Grime, J.P., 1979. Plant Strategies and Vegetation Processes. Wiley, Chichester, 222 pp. Haag, R.W., 1983. Emergence of seedlings of aquatic macrophytes from lake sediments. Can. J. Bot., 61: 148-156. Hannan, H.H. and Dorris, T.C., 1970. Succession of macrophyte community in a constant temperature river. Limnol. Oceanogr., 15: 442-453. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London. Howard-Williams, C., 1978. Growth and production of aquatic macrophytes in a south temperature saline lake. Verb. Int. Verein. Limnol., 20:1153-1158. Howard-Williams, C. and Allanson, B.R., 1981. An integrated study on littoral and pelagic primary production in a Southern African coastal lake. Arch. Hydrobiol., 92: 507- 534. Hunt, R., 1978. Plant Growth Analysis: Studies in Biology, no. 96. E. Arnold, London, 67 pp. Jansson, B.O. and Wulff, F., 1977. Ecosystem analysis of a shallow sound in the northern Baltic - a joint study by the Ask/5 group. Contrib. Askti Lab. Univ. Stockholm, 18: l-160. Kautsky, L., 1987. Life cycles of three populations of Potamogeton pectinatus L. at different degrees of wave exposure in the Aski3 Area, Northern Baltic proper. Aquat. Bot., 27:177186. Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos, 53:126-135. Kemp, W.M., Lewis, M.R. and Jones, T.W., 1986. Comparison of methods for measuring pri-
LAGAROSIPHON IL1CIFOLIUS IN LAKE KARIBA
15
mary production by the submerged macrophyte Potamogeton perfoliatus L. Limnol. Oceanogr., 31: 1322-1334. Lrv~que, C., Dejoux, C. and Lauzanne, L., 1983. Lake Chad, ecology and productivity of a shallow tropical ecosystem. J.P. Carmouze, J.R. Durand and C. Lrv~que (Editors). Junk, The Hague. Lipkin, Y., Beer, S. Best, E.P.H., Kairesalo, T. and Salonen, K., 1986. Primary production of macrophytes: terminology, approaches and a comparison of methods. Aquat. Bot., 26: 129142. Machena, C., 1987. Zonation of submerged macrophyte vegetation and its ecological interpretation in Lake Kariba. Vegetatio, 73:111-119. Machena, C. and Kautsky, N., 1988. A quantitative diving survey of benthic vegetation and fauna in Lake Kariba - a tropical man-made lake. Freshwater Biol., 19: 1-14. Machena, C., Kautsky, N. and Lindmark, G , 1989. Metabolism and nutrient dynamics in Lagarosiphon ilicifolius in tropical Lake Kariba. In: Ecology of the Hydrolittoral Macrophyte Communities in Lake Kariba, Ph.D. Thesis, University of Uppsala. McLachlan, A.J. and McLachlan, S.M., 1971. Benthic fauna and sediments in the newly created Lake Kariba (Central Africa). Ecology, 52: 800-809. Mitchell, D.S., 1969. The ecology of vascular hydrophytes on Lake Kariba. Hydrobiologia, 34: 448-460. Mitchell, D.S., 1970. Autecological studies of Salvinia aurticulata Aubl. Ph.D. thesis. University of London. Morgan, M.D. and Kitting, C.L., 1984. Productivity and utilization of the seagrass Halodule wrightii and its attached epiphytes. Limnol. Oceanogr., 29:1066-1076. Murray, L. and Wetzel, R.L., 1987. Oxygen production and consumption associated with the major autotrophic components in two temperate sea grass communities. Mar. Ecol. Progr. Set., 38: 231-239. Pelican, J. Hudec, K. and Stastny, K., 1978. Animal populations in fish pond littorals. In: D.D. Dykyjov~t and J. Kv~t (Editors), Ecological Studies 28 Pond Littoral Ecosystems. Structure and Function. Springer, pp. 74-79. Rich, P.H., Wetzel, R.G. and Van Thuy, N., 1971. Distribution, production and role of aquatic macrophytes in a southern Michigan marl lake. Freshwater Biol., 1: 3-21. Riemer, D.N., 1984. Introduction of Freshwater Vegetation. AVI Publishing Co., Westport, CT. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular plants. E. Arnold, London, 610 pp. Solander, C.D., 1982. Production of macrophytes in two small, sub-arctic lakes in northern Sweden. In: J.J. Symoens, S.S. Hooper and P. Compare (Editors), Studies of Aquatic Vascular Plants. Royal Botanical Society of Belgium, pp. 181-186. Van Wijk, R.T., 1983. Life cycles and reproductive strategies of Potamogeton pectinatus L. in the Netherlands and the Camargue (France). Proceedings International Symposium of Aquatic Macrophytes, Nijmegen, 18-23 September, 1983. Voilenweider, R.A., 1974. A Manual on Methods for Measuring Primary Production in Aquatic Environment. IBM Handbook, no. 12. Blackwell, London, 213 pp. Westlake, D.F., 1975. Primary production of freshwater macrophytes. In: J.P. Cooper (Editor), Photosynthesis and Productivity in Different Environments. Cambridge University Press, pp. 189-206. Wetzel, R.G. and Hough, R.A., 1973. Productivity and role of aquatic macrophytes in lakes. An assessment. Pol. Arch. Hydrobiol., 20: 9-19.