Read CATTANEO, A., AND J. KALFF. The relative contribution of aquatic macrophytes and their epiphytes to the production of macrophyte beds text version

Limnol. Oceanogr., 25(2), 1980, 280-289 @ 1980, by the American Society of Limnology

and Oceanography,

Inc.

The relative contribution of aquatic macrophytes and their epiphytes to the production of macrophyte beds'

Department of Biology, 1205 Avenue Mont&al, Q&bec H3A 1Bl Ahtmct The cpiphyte contriblltion to the total production of Lake Memphremagog macrophyte beds changed in a predictable fashion with the season, the morphology of the macrophytes, the depth of the bed, and the trophy of the water. In the mesotrophic portion of the lake, epiphytes fixed more carbon than the macrophytes only at the beginning and end of the growing season, whereas under more eutrophic conditions they did so even during summer. Docteur Penfield, McGill University,

Epiphytes always coat aquatic macrophytes. The production of these epiphytes is readily available to grazers whereas that of the macrophytes apparently remains largely unutilized until the plants become senescent at the end of the growing season (Smirnov 1958; Sozska 1975). Macrophyte production should thus contribute significantly to the food supply oc` herbivores and detritovores only late in the season, whereas epiphyte production could sustain grazers throughout the growing season. If these algae form a substantial food base for the browsing community throughout summer and fall, macrophyte control measures may have large and unexpected effects on both primary consumers and their fish predators. Little is known about the relative productivity of macrophytes and epiphytes. Some investigators have been interested only in the macrophytes and have therefore attempted to remove the epiphytes (Wetzel 1964; Adams et al. 1974); others were interested only in the epiphytes and therefore measured their production after removal from the macrophytes (Hickman 1971; Kowalczewski 1975) or by growing them on artificial substrates (Allen 1971). These differences in techniques make results difficult to compare and obscure any synergistic effects due to competition (Fitzgerald 1969), shading (Sand-Jensen 1977), or the exchange of nutrients (1McRoy and Goering 1974).

1 Contribution Lake Memphrcmagog Limnology Kcsenrch Group.

It is our purpose to assess the relative in situ productivity of macrophytes (principally Myriophyllum spicntum and Potamogeton richardsonii) and their undisturbed epiphytes as a function of season, species of macrophyte, depth below the surface, and total phosphorus conccntration of the water. Our data allow an assessment of how these factors affect the epiphyte contributions to the total production of macrophyte beds. The work was largely done in McPherson Bay (45"06'N, 76'16'W) in the central basin of Lake Memphremagog (Qubbec-Vermont) between June and November 1977. We acknowledge a Qukbec Ministry of Education team research grant to the Lake Memphremagog project, a Natural Sciences and Engineering Research Council of Canada grant to J. Kalff, and a Qudbec Ministry of Education scholarship to A. Cattaneo. R. Peters provided advice and J. Smol assisted in the field.

Methods Macrophytes rooting at a depth of 60120 cm were selected for estimating macrophyte and epiphyte production and for determining epiphytic biomass. Because time for colonization influences epiphytic biomass (Cattaneo and Kalff I978), neither the new tips nor the old parts of the macrophyte were sampled; samples were taken about halfway between the sediment surface and the plant tips. To determine the effect of water column depth we also sometimes measured Project, production rates from plants rooting at 280

Production

of mncroghytes

281

water depths ranging from 0.5 to 3.0 m. These experiments necessarily confound the effects of the depth of the water column (total depth) and the depth below the surface at which the samples were taken (sample depth) because macrophytcs growing at different depths do not necessarily reach to the same distance below the water surface. To separate these two depth effects we examined differences produced at deep and shallow sample depths for plants in the same total depth of water and also differences induced by changes in total depth when the same (shallow) sample depth was used. We compared the effect of macrophyte species by comparing the two major species, M. sy>iccltu`rn and P. richardsonii, with each other and with Vallisnericc americana which we sampled on three occasions, The colonization of plastic mimics of these plants (Cattaneo and to deterKalff 1979) was also followed mine if differences among the natural plants reflect their obvious physical differences or some more subtle biotic effect. Finally, we examined the effect of nutrient concentration by comparing production and biomass of epiphytes and production of M. spicntum growing in about 1 m of water at four sites that differ considerably in P concentration, Primary prodlsction of macrophytes and their epiphytes was measured with a "C technique (Cattaneo and Kalff 1979). At each depth and site three to five replicates of each species of macrophyte were incubated in situ in Plexiglas boxes (10x 8 x 8 cm; vol 660 ml) divided longitudinally in half. The box could be closed around a selected portion of the plant with minimum disturbance. A neoprene strip attached to the edge of half of each box ensured a good seal without damage to the stem of the plant when the halves were pressed together. The chambers were held closed by a rubberband and kept in position by small Styrofoam floats. 14C (4-8 @i) as NaH"`C0, was injected with a syringe needle inserted through the neoprene strip; a preliminary dye ex-

periment showed that complete mixing was achieved immediately. After a midday incubation of 34 h, plant stems were cut and the chambers were taken to the sllrface where they were gently opened. The enclosed segments of plant, with their epiphytic cover, were placed in separate vials filled with filtered lake water (Gelman type A-E, glass-fiber filters) and kept in the dark until analysis (l-2 h later). All field manipulations were performed by a SCUBA diver. In the laboratory, the vials were shaken vigorously about 100 tirnes. This separated each sample into two fractions-the detachable epiphytes now dispersed in the water and the plant with its remaining, tightly held epiphytes. The latter could not be separated by scraping the macrophyte because some epiphytes remain attached and the epiphyte samples became contaminated with macrophyte tissue. Our procedure separates the epiphytes into two categories-loose and tight-which differ in species composition, seasonal importance, and, possibly, ecological significance (Cattaneo and Kalff 1978): these categories represent the epiphytes that are or can be removed and those that remain and are, therefore, included in most measurements made by workers interested in aquatic plants. Samples of epiphyte suspensions (i.e. loose epiphytes) were filtered through membrane (Millipore, 0.45 pm) or glassfiber filters (Gelman type A-E) for measurements of primary production OI chlorophyll concentration, The plant segments with their tightly attached epiphytes were immediately dried in an oven at 70°C and later weighed. After they were ground in a mortar, subsamples were combusted (Oximat-Intcrtechnique). The "`CO, evolved was collected in Oxifluor-CO, (NEN) and counted in a scintillation counter (Beckman). Both membrane filters and dried plants were fumed in HCl for 10 min to eliminate Ca1"C03 precipitated during the incubation by macrophyte photosynthetic activity (Wetzel 1965). Membrane filters, which were rolltinely counted with a gasflow colmter (Nuclear-Chicago), were oc-

282 casionally

Cattaneo

und Kulff

recounted with the scintillaafter combustion to assure that methods used for macrophytes and epiphytes yielded comparable results and that self-absorption in those epiphyte samples counted in the Geiger-MG&r system was negligible, Primary production rates were c&ulated following the methods of Vollenweider (1975). Solar radiation was measured with a recording pyranometer (Yellow Springs Instr., model 14138), and daily production rates were extrapolated from the ratio of photons received during the incubation over total photons for that day. Incubations were performed on both cloudy and sunny days; we did not try to standardize the data for the effect of cloud cover, Dark uptake was measured on several occasions, but 8s it accounted for only 2 and 1% of the light uptake of epiphytes and of plants, we disregarded it in our production calculations. Chlorophyll CLof loose epiphytes was determined after correction for pheophytin (Strickland and Parsons 1972). Glassfiber filters were kept frozen until analysis, then ground in 90% acetone and the fluorescence read, before and after acidification, with a Turner fluorimeter which was calibrated against a spectrophotometer (model 88, Bausch and Lomb). Because diatoms are the major component of the epiphytic community in Lake Memphremagog (70-90% of the biomass: Cattaneo and Kalff 1978), and are easily counted after oxidation of the plant material, we used them to estimate the relative proportion of loose and tight epiphytes. Samples of the epiphyte suspension and of plants with their tight epiphytes were boiled in H,SO.I and then IINOs. After several rinsings in distilled water, diatom f'rustules were mounted in Ilyrax (Custom Research and Development) and counted under oil immersion, Volumes of these diatoms were calculatcd by approximation to geometrical solids of similar shapes. All data for production, chlorophyll II, and diatom volume are expressed per unit dry weight of plant. We calculated conversion factors to transform dry weight

tion technique

into area of substrate, experimentally, to make more comparisons with the literature, Surface area of P. richardsonii was &ained by tracing the contour of the b;;tvt~, Myriophyllum sp&turn leaves were CU-t: into small, approximately cylind&al segments the length and diameter of which were measured with an ocular micrometer. The area of the leaves was calculated by assuming that the leaves were cylindrical. The leaves were then dried and weighed. Although varying considerably according to the season and condition of the plants, the conversion factors averaged 0.76 cm2* mg dry wt-1 for M. spicutum and 0.77 for P, richardsonii during midsummer. Temperature, alkalinity (by titration), pH, total P, and reactive Si (according to Strickland and Parsons 1972) were determined from unfiltered water samples collected near the sampled vegetation.

Resul Es and discussion Senson-Both production and biomass of the loose epiphytes were high early in the season, declined sharply in midsummer and increased again in autumn (Fig. 1). Because macrophyte production per unit dry weight did not change drastically over the season, the relative contribution of loose epiphytes on M. spicntum and P. richurdsonii was greatest in June (62 and 30% of total production) and in October-November (60 and 20%>, and minimal in midsummer (4 and 2%). The contribution of the tight epiphytes could only be estimated by comparing the volume of diatoms left on the macrophytes after shaking to the volume of those removed (Table 1). The estimate assumes that production per unit of volume is the same for the loose and ti.ght assemblages and that diatoms are equally well represented in the two epiphyte fractions. Although we do not have data to support the first assllmption, the second one seems valid at least until midsummer when development 01 green and bluegreen algae. became more important in the tight fraction (Cattaneo and Kalff 1978). At that time the contribution of tight epiphytes, based on diatom volume,

Production

MYRIOPH YL LUM SP/CATUM ,

of macrophytes

283

Table 2. Physical-chemical characteristics of McPherson Bay during 1977 growing season. Water collected near sampled vegetation (depth 60-120 cm).

Alkalinity Temp ("C) PII c'l% liter-13 Reactive Si (mg SiOz, liter-`)

loose epiphytes tight eplphytes plant , J J A S 0 N

POTAiWOGE TON

RICHA ROSOA'II

11 Jun 18 Jun 24 Jun 7 Jul 14 Jul 23 Jul 1 Aug 7 Sep 22 Sep 5 Ott 26 Ott 15 Nov

14.0 18.0 19.5 22.5 22.0 23.0 23.0 19.0 17.5 15.0 10.5 6.5

8.5 8.4 8.5 8.5 8.0 8.0 -

45.0 45.2 46.3 45.7 46.6 46.8 -

16.4 14.1 11.4 9.1 16.2 11.0 9.2 10.9 11.3 14.1 s.4

3.06 2.46 2.27 2.34 2.18 270 2.85 2.83 -

Fig. 1. Seasonal changes in primary production of' M. spicntum and P. richardsonii and their epiphytes in McPherson Bay (L. Mcmphremagog) during 1977. Biomass (as Chl n) of loose epiphytes shown on upper panel of each graph. Bars represent SE, n = 3.

could have been underestimated. The biomass of tight epiphytes is seasonally less variable than that of the loose community (Table 1, Fig. 1). IIowever, their

Table 1. Numbers and volumes of tightly attached their pcrccntage of total epiphyte diatoms on different phrcmagog, 1977.

contribution to the total epiphytc biomass ranges from a low of 6% when loose epiphytes are most important, in spring and fall, to a maximum of 68% in midsummer, The seasonal pattern of high epiphyte biomass and production in spring and fall and a lower one in summer had been observed on P. richardsonii in the previous 2 years (Cattanco and Kalt`f 1978, 1979). Sllch R seasonal pattern seems to be widespread and apycars in communities of epiphytes (Pieczynska and Szczepanska 1966), algae on slides (Castenholz

diatoms (i.e. those left on plant after shaking) and dates, macrophytes, and locations in Lake Mem-

Tight No, cells x 105 Macrophyte Location mg plant

diatoms vo,llc.;) dry wt

Tight diatoms ----% Total diatoms No. cells Vol

24 23 24 23 26

Jun Jul Jun Jul Ott

P. rkkwdsonii F. richnrdsonii M. spica turn M. spicntum M. spicatum M. spicatum spice tuna M. spicntum M, spicn turn

McPherson McPherson McPherson McPherson McPherson

Bay Bny Bay Bay Bay

38.6 106.6 464.7 317,7 264.4 288.8 719.6 200.0 152.7

9.6 27.4 75.7 46.7 72.4 171.3 59,8 48.4 51.1

5 49 23 70 15 47 10 41 49

6 64 21 68 19 4: 42 52

15 Nov 8 Scp 8 Scp 8 Scp

Newport McPherson (inflow) Bay Indian-Pcndcr (3 km from inflow) Cove Island Bay (8 km from inflow)

284

Cattuneo

and Kalff

Table 3. Epiphyte biomass and production and macrophyte production for three species of macrophytcs collected in McPherson Bay during slnnmer 1977. Probability that observed differences between consecutive pairs on each linc occurred by chance alone given by P (Wilcoxon signed-rank test, n = 11: Conover 197 1).

M. spicntum P. riclwrdsonii V. umericuna

Epiphyte mg Chl (1*g plant-' mg C-g plant-`*d-l 1'1ant mg C-g plant-`ad-'

0.888 1.26 15.35

P = 5%" P = l%* P = 25%

0.061 0.66 18.35

P = 1%" P = 1%" P = I%*

0.033 0.39 28.00

1960), epipelic algae (Round 1953), and planktonic diatoms (Lund 1950). The pattern is not easily explained. We failed to correlate various physical and chemical parameters (Table 2) with the epiphyte cycle, and wave action too seemed to have little e[fcct (Cattaneo and Peters in prep.). The low summer values may well reflect an increased grazing pressure (Brook 1975) by th c rich f&ma of chironomids, oligochaetes, littoral cladocerans, and snails. Although their role in the seasonal cycle is only now being tested (Cattune0 and Kalff in prep.), their presence suggests an important role for aquatic invertebrates in the removal of epiphytic producti on. Macrophyte species-The loose epiphytic cover was always greater on 2M. spicatum than 011P. richardsonii (Fig. 1). On nearby V. americana, sampled on three dates in midsummer, epiphyte hiomass and production was even lower than on P. richardsonii (Table 3); conversely, macrophyte production per unit dry weight was highest for V. americana and lowest for M. spicatum. Thus at least

Table 4. Epiphytes biomass (Chl (1, mg*me2) per unit leaf surf&e on plastic leaves after 2 weeks of colonization (16-30 July 1977) at two locations in Luke Memphremagog. Significant diffcrenccs Found between Myriophyllum and Vdisnerin (P = I%), Eloden and Potamogeton (P = I%), Eloden and Vnllisneritr (P = 1%) (Wilcoxon signed-rank test, n = 9: Conovcr 1971). Myrilhhu ophyllytn

Potumogeton

Vnllisnericr

McPherson Bay Newport Bay

0.36 2.27

0.36 1.96

0.17 1.89

0.27 0.76

in midsummer the contribution of loose epiphytes to the total production was very low (l-2%) on Vallisneria but more significant 011 MyriophyZZum (4-13%). Other workers have also noted higher epiphyte biomass (Foerster and Schlichting 1965) and production (Kowalczewski 1975) on Myriophyllum than on other macrophytes. This genus also seems to harbor more aquatic invertebrates than Potamogeton, which, in turn, carries greater numbers than Vallisneria (Kreckcr 1939; Andrews and Hasler 1943). We investigated the problem of whether the pattern of high epiphyte biomass on some spccics and low biomass on others is simply a function of the morphology of the leaves (Harrod 1964) by using similarly shaped plastic plants. Plastic V&sneria, Potamogeton, Elodea, and Myriophyllum (Hagen, Mont&al), characterized by an increasing leaf dissection, were planted in two locations. After 2 weeks of colonization Myriophyllum and Elodea, which had the most highly dissected leaves, had accumulated a significantly higher biomass than the other two species (Table 4). Depth-When the production of epiphytes and macrophytes was compared as a function of the depth of the water column (i.e. total depth), we found that the average epiphytic production per gram of macrophyte increased with rooting depth (Fig. 2). IIowever, the average macrophyte production tended to be higher among plants growing in shallow water (Mann-Whitney test, P = 5%, n = 33). The effects of different total depths on plants from constant sample depth and

Production

of macrophytes

SP/CA TUM

285

MYRI OPHYLL UM DEPTH, (cm) 55 100 130 150 195 16 JULY

I

65 125 215

I AUGUST

I

II0 200 280

5 OCTOBER

--=-----

I

I

I

I

1

IO mg C/g

20 plant/day

0.5

I.0 mg Chl a/g plant

1.5

POTAMOGETON DEPTH, (cm) 60 90 140 185

t?/C#AR'OSOff//

I4 JULY

I

90 150 I8 5 215

22

SEPTEMBER

mg C/g

plant/day

mg Chl a /g

plant

Fig. 2. Effect of total water column depth on primary production and loose epiphytes (stippled) of M. spicatum and P. richardsonii. shown on right. Bars represent SE, n = 3.

of plant plus tight epiphytes (striped) Biomass (as C%i a) of loose epiphytes

286

Cattaneo

and Kalff

Table 5. Effects of variations in water column depth and sample depth on A (epiphyte biomass, mg Chl (1-g plant-l), B (epiphytc production, mg C*g plant-`), C (epiphyte specific production, mg Cemg Chl a led-l), and D (plant production, mg C. g plant -`). Values are means of six replicates collected 1 August and 5 October 1977. Mann-Whitney test (Conover 1971) was used to compare effect of total depth when sample depth was constant (first two entries of col. 2) and to compare effect of variations in sample depth when total depth was held constant (last two entries of col. 1). All comparisons showed significant differences (P = 576, n = 1 l), except pairs joined by brackets. -~

Depth total (cm) SClIlll,lC A B C D

$ 6oj \ 5 i \

5 km IO from inflow I5

8 SEPTEMBER

85 165 165

25 25 105

0.187 3.04 0.474 9.78 0.410 1 4.60

18.51 24.34 1 12.84

18.98 16.20 1 16.65 1

5 km

IO from inflow

15

spictltunz

Primary production of Myriophyllum and its epiphytes collected in various bays along nutrient gradient in Lake iMemphrcmngag. Phosphorus concentration declines from 40 to 12 pg P .litcr-' from inflow at Newport to McPhcrson Bay at 18 km. Upper panel of each graph tlcpicts loose cpiphyte biomass (as Chl a). Bars reprcscnt SE, n = 5.

Fig.

3.

of different sample depths on plants with constant total depth were investigated on 1 August and 5 October. Samples of M. qicatum were collected near the upper and lower margins of the bed instead of at its middcpths (Table 5). When total depth was the same, epiphytes growing on that portion of the plant close to the water surface showed a significantly Ilighcr production per unit of macrophyte than epiphytes growing at greater sample depths. This is also reflected in the significantly higher specific production of these shallow water epiphytes, slzggesting an effect oflight. More surprising was that epiphytes growing on plants rooted in deeper water had significantly higher biomass and production than epiphytes growing at the same depth below the lake SUI-fiw~ but on plants in the shallower part ot' the bay. A higher biomass and,

sometimes, a higher production of epiphytes and epilithic algae from deeper water has been reported (Kowalczewski 1975; Schindlcr et al. 1973) and has been attributed to more severe wave action by Fox et al. (1969) and to more intense grazing pressure in shallow waters by Efford (1972). Although we have no evidence for or against these hypotheses, we do predict that macrophyte beds in deeper waters will have a higher epiphytic cove1 and that within any one bed there will be more epiphyte development on segments of plants closer to the water surface. To find out whether the Phosphorusnutrient gradient in Lake Memphremagog (Nakashima et al. 1977; Peters 1979) is also reflected in the prodllction of M. spicatum and its epiphytes we sampled this species at a water depth of about 1 m along the gradient. Biomass (as Chl U) and production of loose epiphytes per unit dry weight of macrophyte were highest at the high P inflow and decreased thereafter (Fig. 3), resulting in a significant correlation with the total P in the water (Fig. 4). Consequently, the significance of loose epiphyte production to total macrophyte production was greater at the inflow (48% in July, 53% in September) than in phosphorus-poor McPherson Bay (13% in July, 4% in September). However, the

Production

of macrophytes

7. 46

I

IO Total

30 P (~g/liter)

50

IO Total P

30 ( Irg /liter

50 )

Fig. 4. Correlations between total P in water and loose epiphytes primary production (left) and chlorophyll (right). Data obtained in various bays with different trophic conditions in Lake Memphremngog, d&-i& summer 1977.

production of the macrophytes, including their tight epiphytes, did not change greatly along the gradient and was therefore not significantly correlated with the total I' in the water. Whether the absence of a macrophyte production pattern was attributable to the macrophytes themselves or to their tight epiphytes was investigated on 8 September when both the loose and tight epiphyte production was estimated from the biomass of the loose and tight diatom fractions (see methods and l'able 1). Both tight and loose epiphytes were particularly pronounced in the high P area (Fig. 3). When the production of tightly attached epiphytes was subtracted, macrophyte production appeared to increase with decreasing total P in the most nutricnt-rich portion of the lake (Fig. 3). Phillips et al. (1978) noted, under laboratory conditions, that a nutrient increase in the water resulted in suppression of a macrophyte ([email protected]) and enhancement of epiphyte growth; he advanced the hy-

pothesis that under progressively more eutrophic conditions massive epiphyte growth could cause macrophyte declines. Depression of plant production by dense epiphyte shading has been reported by Sand-Jensen (1977). Our results show that high nutrient conditions favor epiphytes more than macrophytes. Our data show a high correlation of total phosphorus with summer loose cpiphyte production and with biomass (Fig. 4). These relations promise to be useful in predicting the effect of total P changes on the dynamics of macrophyte beds. Conclusions Our results show that epiphytes synthesize a significant fraction of the production of macrophyte beds. Their absolute importance changes with the season, the morphology of the macrophyte species, the depth of the bed, and the trophy of the water. In the mesotrophic portion of Lake Memphremagog, and probably in similar lakes elsewhere, the loose

288

Table 6. Epiphytc cmergcnt, suhmcrged

Cattaneo

and Kalff

(plant ~111sepiphytes) in beds of

production as a percentage of the total production macrophytes and mosses reported elsewhere.

Epiphytes production %

Plan1

Location

Reference

Ulricdarin Submerged

macrophytes

Everglades, Florida Kalgaard, Denmark Latnajjaure, Lapland Lawrence, Michigan Poland Mikolajskie, Mikolajskie, Poland Fish pond, Czechoslovakia

>50 2 17 30 29 48 21

Mosses (Marsupella) Submcrgcd + emergent mncrophytcs Emergent macrophytes Submerged macrophytes Emergent macrophytes

Brock 1970 Sendergaard and Sand-Jensen 1978 Bodin and Nauwerck Wetzel et al. 1972 Kajak et al. 1972 Kajak et al. 1972 Stra~kraba 1963

1969

epiphytes fix more carbon than the macrophytes during spring and fall whereas under more eutrophic conditions they probably do so throughout the growing season. Previous studies (Table 6) were only addressed to the loose epiphytes but still showed that these normally contribute a significant portion of the total production. Since tightly attached epiphytes produce a substantial fraction of epiphyte production, and since much of the loose epiphytc biomass is readily lost unless extreme caution is taken during sampling, it is likely that in most of these studies the role of epiphytes in macrophyte beds As the macrohas been underestimated. phytes seem to be little grazed by herbivores (Smirnov 1958; Sozska 1975), the contribution of epiphytes to the energy flow in macrophyte beds will be even larger than their contribution to the primary production and may thus be of considerable significance in the productivity of littoral zones. Re&rences

ADAMS, M. S., J. TITUS, AND M. MCCRACKEN.

1974. Depth distribution of photosynthetic activity in a Myriophyllzm spicnturn. community in Lake Wingra. Limnol. Oceanogr. 19: 377390. ALLEN, I-1. L. 1971. Primary production, chemoorganotrophy and nutritional interactions of cpiphytic algae and bacteria on macrophytes in the littoral of a lake. Ecol. IMonogr. 61: 97-127. ANDREW& J. D., AND A. D. IIASLER. 1943. Fluctuations in the animal populations of the littoral zone in Lake Mendota. Trans. Wis. Acad. Sci. 35: 175-185.

BODIN, K., AND A. NAUWEHCK. 1969. Produktionsbiologische Studien tiller die Moosvegetation eincs klaren Gebirgssees. Schweiz. Z. IIydrol. 30: 318-352. BROCK, T. D. 1970. Photosynthesis by algal cpiphytes of Utricularia in Everglades National Park. Bull. Mar. Sci. 20: 952-956. BROOK, A. J. 1975. Aquatic animals aren't hungry in winter, or why Cymhella blooms hcneath the ice. J. Phycol. 11: 235. CASTENHOLZ, H. W. 1960. Seasonal changes in the attached algae of freshwater and saline lakes in the Lower Grand Coulee, Washington. Limnol. Oceanogr. 5: l-28. CAT?'ANEO, A., AND J. KALFF. 1978. Seasonal changes in the epiphyte community of natural and artificial macrofihytcs in Lake Mcmphremagog (@le.-Vt.), Hydrobiologia 60: 135-166. -, AND -. 1979. Primary production of algae growing on natural and artificial aqllntic plants: A study of interactions between cpiphytes and their substrate. Limnol. Oceanogr. 24: 1031-1037. CONOVER,W. J. 1971. Practical nonparametric statistics. Wiley. EFFORD, I. 1972. An interim review of the Marion Lake Project, p. 89-109. Zn Z. Kajak and A. IIillbricht-Ilkowska [eds.], Productivity problems of freshwaters. Pol. Sci. FITZGERALD, G. P. 1969. Sornc factors in the competition or antagonism among bacteria, algae and aquatic weeds. J. Phycol. 5: 351-359. FOERSTER, J. W., AND II. E. SCIILICHTINC, JR. 1965. Phyco-periphyton in an oligotrophic lake. Trans. Am. Microsc. Sot. 84: 485-502. Fox, J. L., T. 0. ODLAUG, AND T. A. OLSON. 1969. The ecology of periphyton in western Lake Superior. 1. Taxonomy and distribution. Bull. Water Resour. Res. Center 14. Univ. Minncsota. 99 p. HARROD, J. J. 1964. The distribution of invcrteln-ates on submerged aquatic plants in a chalk stream. J. Anim. Ecol. 33: 335-348. HICKMAN, M. 1971. Standing crop and primary productivity of the cpiphyton of two small ponds in North Somerset, U.K. Oecologia 6: 238-253.

Production

KAJAK, Z., A. HILLBRIcHT-ILK~~~KA,

of macrophytes

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Submitted: 14 June 1979 Accepted: 5 October 1979

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CATTANEO, A., AND J. KALFF. The relative contribution of aquatic macrophytes and their epiphytes to the production of macrophyte beds

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CATTANEO, A., AND J. KALFF. The relative contribution of aquatic macrophytes and their epiphytes to the production of macrophyte beds