Respiration, nutrient excretion and filtration rate of tropical freshwater mussels and their contribution to production and energy flow in. Lake Kariba, Zimbabwe.
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Hydrobiologia 331 : 25-32, 1996 . © 1996 Kluwer Academic Publishers . Printed in Belgium .
Respiration, nutrient excretion and filtration rate of tropical freshwater mussels and their contribution to production and energy flow in Lake Kariba, Zimbabwe Martina Kiibus & Nils Kautsky Department of Systems Ecology, Stockholm University, S-106 91 Stockholm, Sweden Received 17 September 1995 ; in revised form 15 February 1996 ; accepted 17 April 1996 ,
Abstract The productivity and ecological role of benthos in man-made Lake Kariba was assessed through the use of P/B-ratios and by measuring the metabolism (respiration, N and P excretion) of the most abundant mussel species (Aspatharia wahlbergi, Corbicula africana and Caelatura mossambicensis) in laboratory experiments . For A . wahlbergi also filtration rate was estimated . The annual production of benthos for the populated 0-12 m interval was estimated at 11 .0 g m -2 yr -1 (shellfree dry weight) of which mussels contributed for 8 .81 g (80%), snails 2 .16 g (20%) and insects 0 .03 g (0 .3%) respectively . The most important mussel species in the lake were Caelatura mossambicensis (4 .97 g m -2 yr-1 ) and Corbicula africana (3 .33 g) . The dominant snail species was Melanoides tuberculata (1 .63 g) . For the total lake, also including deeper unpopulated bottoms, the annual production of benthos was 2 .70 g m -2 yr-1 (shell-free dry weight) . Respiration and excretion varied with temperature displaying a bell-shaped relationship . Metabolic rates in Aspatharia wahlbergi increased about 5 x between 16 .5 °C and the maximum at 34 .0 °C and then decreased again at 39 .0 °C, when the mussels showed signs of severe stress . Metabolism in Corbicula africana had a lower optimum with fairly constant activity between 18 .6 and 29 .2 ° C, rapidly decreasing above this temperature . The average respiration, nutrient excretion and water filtration rates for mussels in Lake Kariba at 25 .2 °C were estimated to about 0 .6 mg 0 2 85 pg NH4-N, 1 .5 pg P04 -P and 0 .51 water filtered h -1 g -1 shellfree dry weight . This gives that a volume corresponding to about the total epilimnion of the lake is filtered by the mussels annually . Further, mussels can be estimated to remineralise 1/4 of the total load of phosphate, and 8 times the total load of nitrogen every year. The population needs 3 .5 x 104 tons of organic carbon for its maintainance, which indicates that about 5% of the annual phytoplankton production is channeled through mussels . We conclude that the mussels, rather than being an important food source for fish, seem to play a large role in the nutrient dynamics of Lake Kariba . Introduction In lake ecosystems benthic fauna is the food basis for production of economically important higher trophic levels such as fish . Invertebrates, both filter feeders and detritus feeders, also play a role in the remineralisation of nutrients (Lewandowski & Stanczykowska, 1975 ; Walz, 1978 ; Dame et al ., 1980; Kautsky & Wallentinus, 1980 ; Stanczykowska & Planter, 1985 ; Kasorzajm, 1986 ; James, 1987, Kautsky & Evans, 1987 ; Okedi, 1990 ; Nalepa et al ., 1991) .
Although bioenergetic analysis holds a potential key to understanding the ecological role as well as functional responses of aquatic invertebrates to environmental changes, few studies have hitherto been made of the metabolism of tropical species at high temperatures (Hart, 1980 ; Clarke & Griffiths, 1990 ; Cockcroft, 1990) . The construction of the Kariba dam in December 1958 created the third largest man-made water reservoir in the world (Balon & Coche, 1974 ; Balon, 1978 ; Beadle, 1981) . The development of the invertebrate
26 fauna has been well documented (McLachlan, 1969 ; Begg, 1970 ; Balon & Coche, 1974 ; Kenmuir, 1980 ; Ramberg et al ., 1987 ; Machena, 1989) . By 1975 mussel beds were well established with the first species to appear being Aspatharia wahlbergi and Corbicula africana, while Caelatura mossambicensis and Mutela dubia seem to have colonized later (Kenmuir, 1980) . The benthic animal biomass in Lake Kariba is high compared to most other lakes, probably due to a lack of predators (Kautsky & Kiibus, in press) . 95 .8% of the biomass consists of mussels, 4 .1% of snails and only 0 .1 % of insect larvae (Machena & Kautsky, 1988) . The aim of the present study was to estimate the metabolism (filtration rate, respiration, N and P excretion) of the most abundant mussel species in order to elucidate the productivity and ecological role of mussels in the lake . For two species we also investigated how metabolic rates varied with temperature .
Material and methods The metabolism experiments were performed at the University Lake Kariba Research Station in Lake Kariba, Zimbabwe during the dry season in October and November using mussels from the macrophyte bed in Kassesse Bay, Lake Kariba. The annual temperature range in that area is 19-30 °C with an average of about 25-26 °C in October (Balon & Coche, 1974) . Respiration and nutrient excretion (NH4-N, P04-P) were therefore measured at 25 .2 °C for different sizes of freshly collected mussels, Aspatharia wahlbergi, Corbicula africana and Caelatura mossambicensis. The size range for C. africana was very narrow as only one size-class, close to the normal maximum size of the mussel, could be found in the lake at the time of the study. For A . wahlbergi and C. africana changes in metabolism (respiration and nutrient excretion) with temperature were also measured, within the temperature range found in the lake (cf . Balon & Coche, 1974) . In the temperature experiments Corbicula and Aspatharia specimens were kept for 24 h in large aerated aquaria at four different temperatures for Corbicula (18 .6, 25 .1, 29 .2 and 32 .4 °C) and six different temperatures for Aspatharia (16 .5, 23 .2, 25 .2, 29 .3, 34 .0, 39 .0 °C) in order to adapt to experimental conditions . The water was changed at regular intervals, when food was also added . In each experiment six 1 .5 1 aquaria with a lid were used ; one control aquarium and five with mussels . Each Corbicula aquarium contained 12-
14 specimens (average weight 14 .6 mg shell-free dry weight ; average length 0 .97 cm) and each Aspatharia aquarium contained one medium sized mussel (average weight 1 g shell-free dry weight ; average length 60 mm) . The duration of the experiments was 8 hours, which was assumed to be short enough to prevent starvation and accumulation effects from excretory products, but, on the other hand, long enough to allow short-term adaptation to experimental conditions . During the experiments, oxygen consumption was measured every hour with a polarographic oxygen electrode (Yellow Springs Instruments 59) modified with a stirring device . NH4-N and P04-P excretion were determined according to standard spectrophotometric methods (Carlberg, 1972) as the difference between start and end values . To get an estimate of the water filtration capacity of the mussels, the clearance rate of Aspatharia wahlbergi was measured at 25 .2 °C in 1 .5 1 aquaria filled with turbid water from the bay (Figure ld) and calculated according to the formula: Clearance rate (dm 3 h - ' g - ') = ((lnC)-lnCj)-S) V T -1 B - ',
where Co is the turbidity determined spectrophotometrically at 350 nm at time To ; C1 is the particle concentration at time TI ; V is the volume of suspension ; T is the time elapsed between measurements minus the time of shell closure ; B is the dry tissue weight of the mussel and S is a sedimentation constant calculated as the mean exponential decline in turbidity in the chambers without mussels (Tedengren et al ., 1990) . After termination of the experiments the mussels were dried at 100 ° C and weighed . All values are expressed per g shell-free dry weight . Production of benthos was estimated using data on biomass of mussels and snails, obtained from a diving survey in 1984 (Machena & Kautsky, 1988 ; Kautsky & Kiibus, in press) . By multiplying the biomass values with production over biomass ratios (P/B-ratios) from literature (Winberg et al ., 1971 ; Zaika, 1973 ; Kenmuir, 1980a; Leveque & Saint-Jean, 1983), the production of the main benthic invertebrate species for the total lake as well as per m-2 of the littoral zone between 0-12 m depth was calculated .
Results The weight specific rates of respiration, nutrient excretion (NH4-N and P04-P) and filtration all decreased
27
Phosphate excretion
Respiration 3
-
-
F -Aspatharia wahibergi 17 Corbicula africana 0 Caelatura mossambicensis
F - Aspatharia wahibergi O Caelatura mossambicensis
2
a .5- 2-N
C
a
0 .5-
-a
0 .
0 0
1
2
3
4
5
6
7
8
0
g dry weight
2
3
4
5
6
7
8
g dry weight
Filtration
Ammonia excretion 1 .2
350
1
F -Aspatharia wahibergi 0 Caelaturs 'mossambicensis 0 Corbicula africana
1 1 1 I I - F - Aspatharia wahibergi
1
T
0 .8
..C ';
0 .6
la 0 .4 100 CEO
0 .2
so 0 I i I I i I I 2 3 4 5 6 7 8 0 1 0
1
2
3
4
5
6
7
8
g dry weight
g dry weight Figure 1 . Respiration, nutrient excretion (P04-P and NH4-N and filtration rate in mussels (Aspatharia wahibergi, Corbicula africana and Caelatura mossambicensis) of different sizes from Lake Kariba measured in the laboratory at 25 .2 °C .
with the size of mussels (Figure la-d) . Aspatharia wahibergi and Caelatura mossambicensis of the same size had similar rates, while the smallest species, Corbicula africana, had a much higher individual rate than
the other species . The species specific relationships are given in Table 1 . Respiration and excretion also varied with temperature displaying a bell-shaped relationship (Figure 2a,b) . Metabolism in Aspatharia wahibergi
28
Temperature ° C Figure 2 . Changes in respiration with temperature of mussels (Aspatharia wahlbergi and Corbicula atricana) from Lake Kariba. Figure 2b .
Changes in nutrient excretion (P04-P and NH 4 -N) with temperature of Aspatharia wahlbergi from Lake Kariba Table 1 . Equations of weight-specific metabolic relationships in lake Kariba mussels . The correlation coefficient R is also given . x is given in g dry weight. See Figures la-d . Respiration, mg 02 g - ' h Aspatharia wahlbergi Caelatura mossambicensis NH4-N excretion, µg NH4-N g -I h-1 Aspatharia wahlbergi Caelatura mossambicensis P04-P excretion, ug P04-P g -1 h - ' Aspatharia wahlbergi Caelatura mossambicensis
.252 Y=0.765 * e -0 -0 .159x y=0.739 * e
R=0.91
n=19
R=0.53
n=8
y=118 .0 * e- 0 .320x y= 83 .78 * e- 0127x
R=0.95 R=0.36
n=19 n=8
y=1 .98 * e- 0 .333x y=2.55 * e -0 .313x
R=0.93 R=0.68
n=19 n=8
R=0.82
n=10
Filtration rate, I g - I h - ' Aspatharia wahlbergi
increased with temperature from 16 .5 °C reaching a maximum at 34 .0 °C and then decreased again . At 16 .5 ° C, activity was slow but continuous and the water was clear with little production of mucus . At 23 .2 and 25 .2 °C activity seemed to be normal with some production of mucus, while at 29 .3 °C and 34 .0 °C the activity was increased with a fairly high mucus production . The mussels also showed signs or stress at 34 .0 °C, moving around in the containers once or twice during the experiments . There were also shorter periods of inactivity when they closed their shells at this temperature . At 39 .0 °C the mussels were severly stressed alternating between active periods when they were `coughing' and moving around and longer peri-
Y=0.590 * e -0 •
1 88 x
ods of total closure and inactivity . Mucus production was very high and the water soon became turbid at this temperature. The pattern of Corbicula africana was rather similar, although the metabolism was fairly constant between 18 .6 and 29 .2 °C, implying a quite broad temperature tolerance . However, above 29 .2 ° C respiration decreased markedly, indicating a lower tolerance to extremely high temperatures than Aspatharia . Excretion of NH4-N and P04-P in Aspatharia showed a similar pattern with about five times increase in rates between 16 .5 and 34 .0 °C, which was followed by a decrease at 39 .0 °C (Figure 2b) .
29 m-2 for littoral area Table 2 . Production of benthic animals in total Lake Kariba and as average per between 0-12 m depth. Total biomass values are calculated from Machena and Kautsky (1988), P/B ratios from 1) Leveque et al . (1977), Leveque and Saint-Tean (1983), 2) Kenmuir (1980) and 3) assumed . Conversion to organic dry wt. for mussels from Kenmuir 1980, and for snails from Leveque et al . (1983) . Total biomass tons lake - '
P/B -ratio
Production
(annual)
tons lake - '
Production gm- 2 org . dry-wt .
Corbicula africana
10431
Caelatura mossambicensis
92086 5490
2 .6' 0 .44 2
27121 40518
3 .33 4 .97 0 .30 0 .21
Species
0 .44 2
2416
5931 113940
0 .29 2
Melanoides tuberculata Bellamya capillata
3867 272
4 .4 1
1720 71775 17014
Cleopatra sp . Biomphalaria pfeifferi
628 20 60
5 .8 1 2 .6'
1580 1633
0 .18 0 .29
53 53
100 304
0 .01 0 .04
Mutela dubia Aspatharia wahlbergi TOTAL MUSSELS
Bulinus sp. Lymnaea natalensis
8 .81 1 .63
4
53
TOTAL SNAILS OTHERS
4925 47
21 20652
0 .01 2 .16
53
TOTAL FAUNA
118840
236 92663
0 .03 11 .00
The average production . calculated from P/B-ratios of benthic animals in the populated littoral zone (012 m), amounted to 11 .0 g m-2 yr -1 (org . dry weight) of which the slower growing mussels accounted for 8 .81 g (80%) and the more highly productive snails contributed 2 .16 g (20%), while insects made up only 0 .03 g (0 .3%) (Table 2) . The most important mussel species in the lake are Caelatura mossambicensis (4 .97 g m -2 yr -1 ) and Corbicula africana (3 .33 g) . The dominant snail species is Melanoides tuberculata (1 .63 g) (Table 2) . Although Biomphalaria pfeifferi and Bulinus spp . only contributed a minor part of the production (0 .05 g altogether), they are important secondary hosts of schistosomea (Beadle, 1981), which are vectors of bilharzia, a common human disease along the shores of Lake Kariba .
Discussion There are a few studies concerning metabolism in tropical areas and the influence of temperature on tropical invertebrates (e .g . Clarke & Griffiths, 1990 ; Cockcroft, 1990 ), but the results from Lake Kariba are in consistence with what has been found in temperate areas, although the temperature optimum is higher in Kariba (cf. Stancykowska et al ., 1976; Rodriguez-Ortega & Day, 1978 ; McMahon, 1979 ; Foe & Knight, 1986) . As
expected, the tolerance for high temperatures is much higher in Lake Kariba species which are used to annual temperature variations ranging from around 19 °C to 30 °C (Balon & Coche, 1974) . In South Africa, e .g ., mussels Choromytilus meridionalis showed similar temperature dependent metabolism as in Lake Kariba with respiration rates increasing with temperature between 12 .5 and 30 °C (Clarke & Griffiths, 1990) . Furthermore, there are numerous studies showing the same pattern of the weight specific rates decreasing with size of the mussels as in our study (Rodriguez-Ortega & Dav, 1978 ; Perez-Camacho & Gonzalez, 1984) . The filtration rates seem to be higher in Lake Kariba (about 500 ml h - ' g - ' for a 1 gramAspatharia (Table 1 and Figure Id)) than in some temperate lakes . In Mikolajskie Lake, Poland, the filtration rates of equally sized mussels were about 100-150 ml h - ' g - ' only (recalculated from Lewandowski & Stanczykowska, 1975), that is four to five times lower than in Lake Kariba . Filtration rates were only measured in Aspatharia but we conclude that these values would probably be valid also for the most common species, i .e . Caelatura, since the other metabolic measures were similar in the two species . Production estimates for benthic invertebrates from other tropical lakes are relatively scarce . For the shal-2 , low lake Chad with a mean biomass of 3 .7 g m
30 production has been estimated at 18 g m -1 yr -1 (Carmouze et al ., 1983) . The corresponding values for total Lake Kariba, also including the deep unpopulated areas, are an average biomass of 3 .43 g m -2 and an average annual shellfree production of 2 .70 m -2 yr-1 . The higher production values in Lake Chad are probably mainly due to the fact that this lake is very shallow and that snails and small mussels with relatively high production rates dominate, compared to Lake Kariba where more slowly growing large mussels completely dominate the biomass . In Lake Nakuru, Kenya, the benthic biomass is only 0 .43 g m -2 , but since it is dominated by chironomids the daily production rates are on an average 40 .1 mg dry wt m -2 (Vareschi & Jacobs, 1984), corresponding to about 14 .6 g m2 yr-1 . The generally higher ambient temperatures in many African waters, relative to temperate environments, potentially enhance development rates and shorten life cycles of African invertebrates . Accordingly, Davies & Hart (1981) suggested that temperature exerts more control over production of African aquatic invertebrates than food supply . The role played by the mussels is roughly indicated by comparing their standing stocks of 114000 tons dry weight (Machena & Kautsky, 1988) with current estimates of total fish biomasses in the lake which are 90 000 tons wet weight of which about 32 000 tons are landed annually as the commercially important freshwater sardine 'Kapenta' (Limnothrissa miodon) (Machena et al ., 1993) . Although the mussel stock may thus contain up to 50 times more protein than the stock of Kapenta this resource is presently not utilised . Although mussels are eaten by fish, e .g . they make up one third of the diet of the cichlids (Machena et al ., 1993), predation seems to have little effect on the standing stocks of mussels . Rather, they may compete with fish for food, since the primary production of the pelagic system constitutes the common food base for both mussels and Kapenta. The most important function of mussels in the lake may be the filtering of organic particles from the water and remineralising and recirculating nutrients back to the primary producers . As filter-feeders the mussels circulate and regenerate large amounts of nutrients, which are immediately available for new primary production as they are excreted in the surface water of the lake . Thus, the mussels speed up remineralization and regenerate nutrients in the photic zone . The magnitude of such an impact can be estimated by multiplying the average metabolic rates (using Aspatharia wahlbergi as a model since the most complete set of data was
available for this species and metabolism was usually in the same range as for Caelatura mossambicensis) by the biomass of mussels . The average respiration, nutrient excretion and filtration rates per h -1 g -1 shellfree dry weight obtained for Aspatharia at 25 .2 °C were about 0 .6 mg 02, 85 pg NH4-N, 1 .5 pg P04-P and 0 .51 water filtered (Figure la-d) . Converting our mussel biomass data of 114000 tons dry weight incl . shells to 17784 tons shellfree dry weight (cf . Kenmuir, 1980), gives that a volume corresponding to the total epilimnion of the lake (i .e . 7 .9 x 10 10 m3 ) is filtered and that 13000 tons total inorganic nitrogen and 230 tons of inorganic phosphorus are remineralised annually by the mussel population . Comparing those measurements to total loading from outside sources, and with the mean retention time of the lake water which is only 3-4 years (Machena et al ., 1993) gives an estimate of the role of mussels in cycling nutrients in Lake Kariba . While the total mean load of phosphorous and nitrogen into the lake is about 1025 tons yr 1 and 1684 tons yr -1 respectively (Magadza et al ., 1989), this means that mussels remineralize about 1/4 of the phosphorous and 8 times the annual inputs of nitrogen . Literature data show that in temperate lakes phosphate turnover may occur approximately 20 times a year (Golterman, 1975) whilst in the Lago Januauaca and several East African lakes it can occur as frequently as every 1-3 hours (Fisher & Parsley, 1979 ; Peters & Maclntyre, 1976) These data include also the remineralization by microbial organisms, zooplankton and other organisms . In Lake St . Clair the mussel population filtered about 13 .5% of the total phosphorous load (Nalepa et al ., 1991) . Mussels may therefore contribute significantly to nutrient cycling in Lake Kariba, especially with regard to nitrogen . Furthermore, the mussel population in Lake Kariba consumes 9 .3 x 104 tons oxygen per year which indicates that it needs 3 .5 x 104 tons of organic carbon for its maintainance (cf. Odum, 1971), which means that about 5% of the annual phytoplankton production is channeled through mussels . As the phytoplankton biomass generally seems insufficient to supply the pelagic food web in Lake Kariba (Machena et al ., 1993), the role of mussels as remineralizers is even more important.
Acknowledgements The study was carried out at the University Lake Kariba Research Station whose staff helped with collection
31 of field material and put laboratory facilities at our disposal . The study was financed by SAREC (Swedish Agency for Research Cooperation with Developing Countries) and SIDA (Swedish International Development Cooperation Agency) .
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