Department of Biology, East Carolina University, Greenville, NC 27834 (U.S.A.) ... University of Maryland, Horn Point Environmental Laboratories, Cambridge, ...
Aquatic Botany, 22 (1985) 231--252
231
Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands
BIOMASS PRODUCTION AND NUTRIENT CYCLING IN AQUATIC MACROPHYTE COMMUNITIES OF THE CHOWAN RIVER, NORTH CAROLINA
R O B E R T R. TWILLEY ~, LACY R. BLANTON 2, MARK M. BRINSON and G R A H A M J. DAVIS
Department o f Biology, East Carolina University, Greenville, NC 27834 (U.S.A.) Contribution No. 82-1483 from the Center for Environmental and Estuarine Studies, University of Maryland (Accepted for publication 6 May 1985)
ABSTRACT
Twilley, R.R., Blanton, L.R., Brinson, M.M. and Davis, G.J., 1985. Biomass production and nutrient cycling in aquatic macrophyte communities of the C h o w a n River, North Carolina. Aquat. Bot., 22 : 231--252. Net primary productivity (NPP) o f Nuphar luteum (L.) Sibth. & Smith and Justicia americana (L.) Vahl was estimated for stands in the Chowan River, North Carolina. NPP of J. americana was estimated at 173 g dry wt. m -2 per growing season, based on the difference between maximum and minimum standing crops. F o r N. luteum, the great variation in biomass estimates and observed high mortality of floating leaves during the growing season resulted in an underestimate o f net production using this approach. Estimates based on tagging experiments were 222 g dry wt. m -2 year -2 using annual turnover rates, compared to 234 g dry wt. m -2 year-1 using monthly rates. Nearly 92% of this net production was accounted for by above-ground structures, although they represented only 33% of the biomass at any one time. Nutrient distributions in both species differed spatially and seasonally for each plant structure, which suggests that accurate estimates o f nutrient turnover would have been masked by whole plant analyses. Most notable, were high affinities of iron in below-ground structures and calcium and nitrogen in above-ground structures for both species. One-half the dry mass of above-ground structures was lost from mesh bags in only 7 days for N. luteum compared to 60 days for J. americana, indicating the high recycling potential of aquatic plant detritus. Nutrient immobilization during decomposition was minor except for calcium and magnesium in above-ground structures of J. americana. Highest nutrient turnover rates were for nitrogen and potassium at about 7.5 g m -2 year -~ in N. luteum and nutrient turnover rates for the floating-leaf macrophyte were higher than for the emergent macrophyte. Assuming that most of these nutrients originated from the sediments, these turnover rates represent significant fluxes of nutrients to the water column.
University of Maryland, Horn Point Environmental Laboratories, Cambridge, MD 21613, U.S.A. 2 Burroughs-Wellcome Corp., Greenville, NC 27834, U.S.A.
0304-3770/85/$03.30
© 1985 Elsevier Science Publishers B.V.
232 INTRODUCTION Net primary productivity (NPP) and nutrient cycling associated with littoral freshwater macrophytes m a y be significant to the function of aquatic ecosystems (Penfound, 1956; Westlake, 1 9 6 5 a ; Wetzel, 1975; Hutchinson, 1975; Brinson et al., 1981). Comprehensive studies that couple biomass distribution and NPP with nutrient content are lacking, particularly for aquatic macrophytes in lentic environments. Problems associated with interpreting existing data on organic matter production include differences in terminology, criteria and m e t h o d o l o g y used (Westlake, 1965b); plus there is a general lack of information concerning below-ground production and biomass (Brinson et al., 1981). Also, nutrient uptake, translocation and secretion m a y be plant specific, as well as different among nutrients for a single species (Brist o w and Whitcombe, 1971; DeMarte and Hartman, 1974). These specific internal flows may cause vegetative (Riemer and Toth, 1970; Cowgill, 1973; Drifmeyer et al., 1980; Kimball and Baker, 1983) and seasonal (Hutchinson, 1975; Nichols and Keeney, 1976; Kimball and Baker, 1983) differences in elemental composition of r o o t e d aquatic plants. Whole plant analyses m a y mask these temporal and spatial variations and together with calculations of biomass turnover, result in inaccuracies in estimates o f nutrient flux in aquatic plant populations. The purpose of this study was to evaluate the NPP, biomass distribution and nutrient concentration of Nuphar luteum (L.) Sibthorpe and Smith and Justicia americana (L.) Vahl, in the littoral zone o f a coastal plain river. The individual plant structures (leaves, roots and rhizomes) of each species, at various sites in the Chowan River, were analyzed to determine the extent that nutrients in separate plant parts varied with site and season. These results were combined with estimates of biomass distribution and NPP to determine the turnover of nutrients and organic matter for an emergent and a floating-leaf m a c r o p h y t e which have different morphological and phenological characteristics. Nuphar luteum, a floating-leaved m a c r o p h y t e bearing submersed leaves with short petioles and floating leaves with long flexible petioles, grows predominantly in monospecific stands. Perennial and sympodial rhizomes of N. luteum are fleshy with large leaf and peduncle scars on their surfaces. Justicia americana is also perennial, b u t is an emergent m a c r o p h y t e bearing leaves almost entirely on erect aerial stems (Fassett, 1972). The coarse rhizomes, superficially similar in m o r p h o l o g y to the erect stems, have roots that foizn dense mats near the surface of the sediments. STUDY AREA AND METHODS The Chowan River, located in the northeastern coastal plain of North Carolina, originates at the confluence of the Blackwater and N o t t a w a y Rivers and flows approximately 81 km to the south into the Albermarle Sound.
233 The sector studied lies between the U.S. Highway 17 bridge near E d e n t o n , North Carolina and extends 52 km northward to the U.S. Highway 13 bridge near Winton, North Carolina (36°03'N to 36°23'N and 76°41'W to 76°56'W). Three sites were sampled intensively for N. luteum ( R o c k y h o c k Creek, Keel Creek and Wiccacon Creek), while only one (Rockyhock Creek) was sampled for J. americana. All sites were located at m o u t h s o f tributaries where aquatic macrophytes are limited to a narrow littoral zone and somewhat p r o t e c t e d from high-energy waves. A quadrat size of 0.35 m 2 was chosen for routine sampling for the two species because previous tests showed it was a compromise between low variance and high labor costs for larger quadrat sizes (Blanton, 1976). In each plant bed, a 30-m transect parallel to shore served as a baseline from which transects were run at r a n d o m points perpendicular to the shore across the width of the m a c r o p h y t e stand. A quadrat frame was placed at r a n d o m points along this line and plant biomass was removed to a sediment d e p t h o f approximately 30 cm. The n u m b e r of samples for estimates of biomass ranged from 4 to 8. The m a c r o p h y t e s were cleaned of periphyton, separated by structure (N. luteum: rhizomes, roots, floating leaves and petioles, submersed leaves and petioles, flowers, peduncles and fruits; J. americana: leaves, stems, flowers and fruits, rhizomes and roots), dried at 85°C for 72 h and weighed. Results are expressed as g m -2 of dry weight. To account for biomass losses due to senescence or damage in N. luteum, all floating leaves were tagged in a 1-m × 12-m quadrat established in a m a c r o p h y t e stand at R o c k y h o c k Creek. Newly emerged floating leaves were tagged weekly beginning with the first emergent leaf of the growing season. By loosely tying plastic flagging with aluminum tags to the floating leaves, weekly records were maintained of the n u m b e r of new leaves emerged and of those lost during the growing season. The n u m b e r of annual leaf turnovers was determined by dividing the n u m b e r of days in the growing season by the average n u m b e r o f days t h a t the tagged leaves were emerged. Using this estimate, productivity for the emergent leaf blades and petioles was calculated by multiplying the average standing crop for leaf blades and petioles for the growing season by the n u m b e r of turnovers (Waring, 1970}. Submersed leaf and flower p r o d u c t i o n was determined in the same manner. NPP of below-ground structures was measured by marking the rhizome tip of the plants used in analysis of floating leaf turnovers with metal stakes at the beginning of the growing season. All growth past this metal stake was harvested at the end of the growing season and designated as seasonal growth. Petiole and peduncle scars were c o u n t e d on this new growth and on the older portion of each rhizome. The total n u m b e r of petiole and peduncle scars divided by the n u m b e r of new petiole and peduncle scars gave an estimate of rhizome age. The n u m b e r of new scars was confirmed by comparing the n u m b e r of newly tagged floating leaves and petioles plus peduncles with the total n u m b e r o f petiole and peduncle scars on the new rhizome growth. Also, total rhizome length divided by the one-year growth increment resulted in an additional estimate of average rhizome age.
234
K o o t p r o d u c t i o n for the growing season was determined b y an indirect m e t h o d , since it was observed that roots posterior to the growing apex progressively increased in length. Estimates of average annual r o o t production, assuming r o o t growth to be proportional to annual rhizome biomass growth, was determined by linear regression of r o o t biomass on rhizome biomass,
Leaf area index (LAI) was determined for both m a c r o p h y t e communities. All live leaves within a 0.35-m 2 quadrat were traced on paper and their surface area determined b y the proportionality: Area of page
Area of leaf
Weight of page
Weight of leaf trace
The dried biomass material was pooled for each date and site and ground with a Wiley mill (40 mesh), except for rhizomes which were pulverized in a blender. Duplicate analyses were run on all samples. Total nitrogen c o n t e n t was determined with a Coleman ® Model 29 nitrogen analyzer. Samples were prepared for cation and phosphorus analyses by ashing 1-g aliquots of each ground sample in a muffle furnace for 3 h at 480°C. After recording ash weight, the ash was dissolved with concentrated HC1, diluted with distilled water and filtered through Whatman®41 filter paper. The filtered residue (presumably silicon) was subtracted from the total ash residue before ashfree dry weight values were calculated. Insoluble ash in the above-ground samples was negligible, b u t an average of 29% of the dry weight of roots was insoluble residue. Phosphorus was determined by the m o l y b d a t e blue procedure for o r t h o p h o s p h a t e (Environmental Protection Agency, 1971) and cation analyses of the filtered solutions were made with a Perkin Elmer ® atomic absorption spectrometer model 305B. Glassware for these analyses was soaked overnight in 2% nitric acid and filter papers were rinsed with distilled water. Plant decomposition was estimated for N. luteum and J. americana using the mesh bag technique ( K o r m o n d y , 1968; Boyd, 1970}. Transects of fiberglass bags (mesh size of 1 mm 2) containing 35 g fresh weight each of either above-ground (leaves and petioles or stems) or below-ground (roots and rhizomes) material were placed at the m o u t h of R o c k y h o c k Creek on 30 S e p t e m b e r 1974. The bags with above-ground vegetation were located on the sandy sediment surface and bags with below-ground plant material were buried at a b o u t 10 cm depth. Duplicate bags were randomly collected for analysis weekly during the first m o n t h and then m o n t h l y for 5 months. Plant material was picked from the collected bags, rinsed, dried for 48 h at 85°C and weighed. Dried plant material was processed and analyzed for nutrients as described above.
235 RESULTS Biomass distribution Peak biomass of N. luteum among three sites occurred during July--September and ranged from 115 g m -2 (Keel Creek) to 300 g m -2 (Wiccacon Creek) (Fig. 1). The mean m o n t h l y biomass value (April--August 1975) for the three sites was 155 g m -2, of which 119 g m - : was below ground. The proportion of total biomass in the sediment varied from a low of 63% at Wiccacon Creek, where the highest peak biomass was measured, to 89% at Keel Creek during November when above-ground biomass was declining (Fig. 1). The below-ground (BG) to above-ground (AG) biomass ratio at peak biomass f o r N . luteum was 2.4. ROCKYHOCK CREEK
KEEL CREEK
WtCCACON CREEK
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JUN 4UL AUG 25 25 20
Fig. 1. B i o m a s s e s t i m a t e s of Nuphar luteurn a t t h r e e sites o n t h e C h o w a n River, N o r t h Carolina.
Justicia americana at R o c k y h o c k Creek reached a peak biomass of 277 g m-: during August with an estimated 42% of total biomass (BG:AG = 0.7) in the sediment (Table I). Uniform growth of above-ground structures (stems and leaves) was observed during the growing season. The biomass present in December was substantial at 206 g m -2. Average biomass for J. americana during the growing season (May--September) was 189 g m -2. The m a x i m u m leaf area index (LAD for N. luteum was 0.82 during August at Wiccacon Creek, c o m p a r e d to only 0.25 at the two other sites. These LAIs correspond to leaf densities o f 31 m -2 and 6 m -2, respectively.
236 TABLE I Summary of monthly biomass (g m -~ -+ S.E.) of Nuphar luteum and Justicia americana. The data for N. luteum are the average for the three sites in Fig. 1 April Nuphar luteum Above ground Floating leaf Floating leaf petiole Submersed leaf Submersed leaf petiole Reproductive structure Sum
Below ground Rhizome Root Sum Total
May
June
July
Aug.
Sept.
Mean
0.2 0.2 5.7 3.5 0 9.6
14.9 10.5 8.8 4.8 0.4 39.4
12.7 13.6 6.4 2.5 1.6 36.8
11.6 15.4 8.0 4.1 0.3 39.4
17.8 20.2 6.5 4.9 3.5 52.9
11.4 12.0 7.1 4.0 1.2 35.7
111.4 22.7 134.1
104.6 21.9 126.5
91.5 21.9 113.4
77.6 18.6 96.2
97.3 21.9 119.2
97.3 21.9 119.2
143.7 165.9 150.2 135.6 172.1 (-+13.0) (±35.5) (-+40.3) (-+46.5) (-+37.2)
154.9
Justicia americana Above ground Leaf Stem Reproductive structure Sum
3.9 18.9 0 22.8
16.6 67.8 0 84.5
24.4 111.8 0.1 136.3
30.4 129.9 0 160.3
12.0 57.9 0 69.9
17.5 77.3 0.1 94.9
Below ground Rhizome Root Sum
71.3 9.0 80.3
59.5 21.2 80.7
72.4 29.3 101.7
86.2 30.0 116.2
70.3 22.3 92.6
71.9 22.4 94.3
162.5 (-+55.4)
188.2
T h e m a x i m u m L A I f o r J. a m e r i c a n a w a s 0 . 6 3 in J u n e a n d m a x i m u m d e n s i t y w a s 2 5 m - : in J u l y a t R o c k y h o c k C r e e k .
stem
Total
103.1 165.1 238.0 276.2 (-+15.6) (-+31.7) (-+65.0) (-+92.4)
Biomass turnover
T h e g r o w i n g season f o r N. luteurn was e s t i m a t e d f r o m e m e r g e n c e o f n e w l e a v e s ( 1 0 M a y ) t o t h e f i r s t f r o s t (2 N o v e m b e r ) f o r a t o t a l o f 1 7 6 d a y s ( F i g . 2). T h e n u m b e r o f n e w l y e m e r g e d l e a v e s p e a k e d b y e a r l y J u n e a n d n o l e a f production was observed after early October; this pattern roughly followed that of the maximum and minimum water temperatures at this site. There was no discernable pattern for dead leaves. From these frequencies of leaf
237
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J . a m e r i c a n a - - below ground ( 12 days) > N. luteum - - below ground (36 days) > J. a m e r i c a n a - - above ground (63 days). Most noticeable changes in nutrient concentration were for K, which decreased in all instances and Ca, which increased by as m u c h as 200% of the original concentration in roots and rhizomes (Table V). Phosphorus and Mg concentrations increased slightly, while N concentrations increased in above-ground structures but decreased in below-ground parts. Based on percentage of original mass of nutrients within the mesh bags, n u t r i e n t immobilization was observed for P, Ca and Mg in leaves and stems of J . a m e r i c a n a . The strongest pattern of n u t r i e n t conservation was observed for Ca in decomposing roots and rhizomes of N . l u t e u m , which had more than 70% of
246
TABLE V
Nutrient concentrations (rag g-~ A F D W ) ~ in decomposing above-ground and below-ground structures of Nuphar luteum and Justicia americana in C h o w a n River. Experiments were initiatedon 30 September at Rockyhock Creek Time (weeks)
Nuphar luteum
Jus ticia americana
Above ground
Below ground
Above ground
Below ground
Nitrogen 0 1 3 4 8 12 18 24
29.2 32.0 32.9 34.9 ND b ND ND ND
16.7 13.7 10.9 12.0 ND 12.2 ND ND
ND ND ND ND ND ND ND ND
ND ND ND ND ND ND ND ND
Phosphorus 0 1 3 4 8 12 18 24
3.83 3.68 2.73 1.95 ND ND ND ND
2.45 3.02 4.68 3.76 3.04 2.82 3.78 2.50
1.37 2.17 0.80 0.76 1.40 1.64 1.37 1.33
2.98 1.98 1.18 1.10 1.32 1.52 1.69 1.51
Potassium 0 1 3 4 8 12 18 24
38.19 24.49 12.12 6.49 ND ND ND ND
36.12 23.72 19.60 12.32 13.87 8.16 8.36 1.57
55.88 48.49 35.14 17.25 23.46 9.33 3.55 1.11
28.39 17.74 2.27 4.11 0.91 0.81 0.72 ND
Calcium 0 1 3 4 8 12 18 24
11.44 17.34 9.97 6.27 ND ND ND ND
3.43 7.71 7.49 7.10 7.60 8.56 11.58 19.03
20.16 51.56 30.27 21.69 12.62 4.03 4.53 4.17
5.23 6.43 13.92 13.20 10.44 ND 5.35 8.11
Magnesium 0 1 3 4 8 12 18 24
2.67 2.04 0.86 0.85 ND ND ND ND
0.82 1.06 1.28 0.84 0.75 0.78 1.22 1.54
8.96 21.08 18.34 4.13 7.65 2.37 1.07 0.69
4.89 5.57 2.65 2.36 0.96 6.12 2.63 2.99
A F D W ffi ash-free dry weight. 2 ND ffi no data available.
247
the original mass remain in the bag t h r o u g h o u t the field incubation. The leaves and petioles of N. luteum a n d roots and rhizomes of J. americana had highest rates of nutrient loss from mesh bags, except for Ca in the emergent macrophyte. DISCUSSION
Adams et al. (1973) observed that r o o t e d aquatic plants varied widely in their capacity to reflect ambient nutrient levels based on whole plant nutrient analyses. Yet Hutchinson (1975) and more recently Kimball and Baker (1982, 1983) have pointed o u t that seasonal, structural and spatial differences occur in the nutrient c o n t e n t of macrophytes, even among plants of the same family at the same site. Results of this study indicate that the advantage gained by among-site comparisons can be m o s t revealing when the individual parts, rather than whole plants, are compared. F o r example, the differences in Fe and P c o n t e n t of N. luteum among the sites of this study w o u l d have been masked if the roots had been pooled with the heavier plant structures. Seasonal changes in the nutrient c o n t e n t o f emergent and floating-leaf m a c r o p h y t e s were nutrient specific and for a particular nutrient these temporal changes were specific for a morphological structure. Nitrogen c o n t e n t in the growing tips of M y r i o p h y l l u m varied during the summer with peak concentrations at the beginning of the growing season (Nichols and Keeney, 1976; Kimball and Baker, 1982, 1983), a p h e n o m e n o n that was observed for the leaves of b o t h J. americana and N. luteurn in this study. However, nutrients in N. luteum exhibited minor seasonal differences compared to the emergent m a c r o p h y t e which m a y be the result of the continuous biomass turnover of leaves and petioles t h r o u g h o u t the growing season. J. americana aged t h r o u g h o u t the growing season and during the latter summer months and early fall, when J. americana senesced, extreme nutrient changes were observed in the above-ground biomass. These results indicate that plant phenology must be considered when evaluating the nutritional status of r o o t e d aquatic plants. The peak biomass of N. luteum ranged from 115 to 300 g m -2. The maxim u m biomass and LAI occurred in the northern portion of the river at Wiccacon Creek, where wave amplitude was small owing to the narrowness of the river. The lowest value of standing crop was observed at Keel Creek in beds growing on a soft organic ooze. The biomass values for N. luteum in this study are among the lower estimates for floating-leaf macrophytes (Bernatowicz and Pieczynska, 1965); and much lower than 1329 g m -2 (Waring, 1970) and 1614--2181 g m -2 ( G o o d and G o o d , 1975) for N. advena Aiton. The lower biomass estimates f o r N . luteum occurred in the lower, less p r o t e c t e d sections o f the Chowan River where LAI was only 0.2, compared to higher estimates in the narrow littoral zone of the upper river where LAI was 0.8. However, these LAI estimates are low compared to Nuphar popula-
248 tions in more lentic environments, such as 4.7 for N u p h a r variegaturn (Nicholson and Best, 1974) and 4.0 f o r N . advena (Waring, 1970}. Peak biomass o f J. americana in this study was lower compared to the same species in Lake Olgletree, Alabama (Boyd, 1969), which m a y also be explained by the much lower density (25 stems m -2 in this study compared to 716 stems m -2 in Alabama). These lower biomass estimates of macrophytes in this study m a y reflect factors associated with lotic environments (e.g, wave stress, currents, nutrient conditions, light, etc.} that inhibit c o m m u n i t y structures that are characteristic of more quiescent waters. Nearly 67% of the total biomass o f N . luteum was in the sediment, which is characteristic of perennial marsh m a c r o p h y t e s (Whigham and Simpson, 1978). Thus a BG:AG ratio of 2.4 compares to 0.86 (Whigham and Simpson, 1978), 1.89 {Good and G o o d , 1975) and 4.25 (Waring, 1970) f o r N . advena. Records on individual rhizomes of N. luteum have suggested a lifespan of more than a century (Heslop-Harrison, 19.55). The average rhizome age in this study was approximately 7 years, s o m e w h a t higher than the rhizome age (4 years} reported in Waring's {1970) study o f N . advena. As pointed o u t by others (Sculthorpe, 1967; Hutchinson, 1975), the ecological role of rhizomes is apparently to furnish energy for asexual vegetative propagation and rapid growth of emergent organs in the spring. Yet, contrary to observations on other emergent m a c r o p h y t e s {Davis and Van der Valk, 1983}, nutrient concentrations in rhizomes did n o t change in the spring in response to above-ground growth. Neither were there obvious increases in nutrient concentration of rhizomes during the fall, when retranslocation o f elements from leaves and shoots to below-ground structures occurs in o t h e r aquatic plant communities. The n u m b e r of floating leaf and petiole turnovers was 5.7 for the 1975 growing season (176 days) in North Carolina compared to 4.4 times per growing season (149 days) for N. advena in Pennsylvania (Waring, 1970). However, the average lifespan of floating leaves and petioles was similar for b o t h N. luteurn {31 days) and N. advena (34 days} in spite of differences in biomass and c o m m u n i t y structure. Biomass turnover estimates from tagging experiments for submersed m a c r o p h y t e s range mostly from 0.5 to 1.5 year -1 (Rich et al., 1971; Sand-Jensen and S~bndergaard, 1978; Moeller, 1978, 1980), with higher values from 2--3 based on productivity estimates {Adams and McCracken, 1974). Annual turnover estimates for above-ground structures of emergent m a c r o p h y t e s also range from 1.2 to 2.4 (Whigham et al., 1978), suggesting that floating leaf m a c r o p h y t e s m a y have characteristically higher annual turnovers of biomass compared to other freshwater and brackish aquatic macrophytes. Estimates of NPP o f N. luteum, based on m a x i m u m and minimum standing crop, were only 17% of the estimates based on biomass distribution and turnover. Above-ground NPP calculations, based on m o n t h l y averages o f leaf turnover and biomass, were 254 g m -2 year -~ compared to 205 g m -~ year -1 using annual leaf turnovers and mean annual biomass. Below-ground produc-
249
tivity was much less at 16.7 g m -2 year -~. The rhizome production of N. luteum during the growing season was estimated by dividing the average seasonal biomass of rhizomes by the average rhizome age. This m e t h o d assumed t h a t rhizomes of different ages had similar growth characteristics and t h a t each year the rhizome meristem grew the same length and produced the same number of petioles as in 1975. Total annual r o o t and rhizome production for N. luteum was only 26.7 g m -2 or 22% of the average belowground biomass for the growing season. The below-ground productivity of N. advena reported by Waxing (1970) was m u c h higher (291 g m -2 year-i); however, this production represented a similar percentage (27%) of the below-ground biomass as observed for N. luteum. By summing all components of NPP, the total value estimated for N. luteum ranged from 222 to 250 g m -2 for the 1975 growing season or 1.35 g m -2 day -~. Although only 33% of the biomass was in above-ground structures, t h e y accounted for 92% of the NPP. Thus, m a x i m u m annual biomass estimates had no relationship to either the magnitude or the distribution of NPP in N. luteum. This estimate of NPP for N. luteum is only one-third the reported values for annual p r o d u c t i o n of N. advena (Waring, 1970; Whigham et al., 1978). Submersed leaves and petioles were present t h r o u g h o u t the year, although annual production was based only on biomass turnover data during the growing season. However, no new submersed leaf production was observed during the winter months. Aquatic insects, white-tail deer and waterfowl grazed heavily upon the fruits and flower parts during the growing season which reduced the seasonal average biomass and, thus, our study underestimates above-ground productivity. Floating-leaf and submersed aquatic plants decompose in 1--3 m o n t h s ( K o r m o n d y , 1968; Nichols and Keeney, 1973; Kistritz, 1978; Godshalk and Wetzel, 1978), which is m u c h faster t h a n emergent macrophytes at 6--12 months (Boyd, 1970; Danell and SjSberg, 1979). Above-ground biomass of N. luteum and J. americana disappeared from mesh bags in 4--8 weeks, respectively, in the littoral of the Chowan River with associated high n u t r i e n t release rates. These results suggest t h a t nutrients accumulated in aquatic plants m a y be quickly recycled in aquatic ecosystems with residence times less than a year, although the remineralization of particulate nutrients < 1 mm 2 is u n k n o w n . Nutrient release from the emergent m a c r o p h y t e occurred during the fall when the above-ground biomass died and decayed. The floating-leaf m a c r o p h y t e recycled nutrients t h r o u g h o u t the growing season, y e t peak mortality turnover rates also occurred in October and November. Approximately 63 g m-: of acid-extractable P is stored in the top 25 cm of sediment in the Chowan River (based on a mean of 4 sites) and the total phosphorus c o n t e n t of the water column at 1 m depth is a b o u t 0.1 g m -2 (TwiUey, 1976). Based on the P fluxes for J. americana and N. luteum, the turnover time for extractable P in the sediments would be 420 and 684 years, respectively. However, considering the lower P c o n t e n t in the over-
250
lying water, residence times are only 0.7 and 0.14 years. These residence times of P would be further reduced by the secretion of P from aboveground structures during the summer, especially submersed leaves (Twilley et al., 1977). Assuming roots supply most of the nitrogen to above-ground structures, nitrogen flux in leaves and petioles represents a flux of 8.0 g N m -2 year -1 (based on a growing season of 176 days) from the sediment. These estimates indicate that because of the high biomass turnover of this floating-leaf aquatic macrophyte, nutrient fluxes equivalent to 2--4 times the nutrient content of below-ground biomass could be transported across the sediment/ water interface per year. None of these flux rates suggest that nutrient supply limits NPP of rooted macrophytes in the Chowan River. As suggested earlier, the lotic nature of our study site may limit the community development and biomass production of aquatic macrophytes, as indicated by their limited distribution only in the most protected habitats of the river. Under these conditions, nutrient supplies would be high and the significance of nutrient recycling minimal in this and other relatively exposed littoral zones of large water bodies. In small, shallow ponds with little wave stress much higher NPP and biomass development for these and associated species may occur and thus these communities would strongly influence nutrient cycling in such aquatic ecosystems. ACKNOWLEDGEMENTS
This research was supported by the Water Resources Research Institute of the University of North Carolina under grant B-079-NC to M.M. Brinson and G.J. Davis and from funds provided by the office of Water Research and Technology, U.S. Department of Interior. J. Gilliard typed the manuscript and J. Metz drafted the figures.
REFERENCES Adams, F.S., Cole, H., Jr. and Massie, L.B., 1973. Elemental constitution of selected aquatic vascular plants from Pennsylvania: submersed and floating leaves species and rooted emergent species. Environ. Pollut., 5 : 117--147. Adams, M.S. and McCracken, M.D., 1974. Seasonal production of the Myriophyllum component of the littoral of Lake Wingra, Wisconsin. J. Ecol., 62 : 457--465. Bernatowicz, S. and Pieczynska, E., 1965. Organic matter production of macrophytes in the lake Taltowisko (Masurian Lakeland). Ekol. Pol., 13: 113--124. Blanton, L.R., Jr., 1976. Primary productivity and biomass distribution of aquatic macrophytes in the lower C h o w a n River. M.S. Thesis, East Carolina University, 85 pp. Boyd, C.E., 1969. Production, mineral nutrient absorption, and biochemical assimilation by Justicia americana and Alternanthera philoxeroides. Arch. Hydrobiol., 66: 139-160.
251 Boyd, C.E., 1970. Losses of mineral nutrients during decomposition of Typha latifolia. Arch. Hydrobiol., 66: 511--517. Brinson, M.M., Lugo, A.E. and Brown, S., 1981. Primary productivity, decomposition and consumer activity in freshwater wetlands. Annu. Rev. Ecol. Syst., 12: 123--161. Bristow, J.M. and Whitcombe, M., 1971. The role of roots in the nutrition of aquatic vascular plants. Am. J. Bot., 58: 8--13. Cowgill, U.M., 1973. Biogeochemistry of rare-earth elements in aquatic macrophytes of Linsley Pond, North Branford, Connecticut. Geochem. Cosmochim. Acta, 37: 2329-2345. Danell, K. and Sj~berg, K., 1979. Decomposition of Carex and Equisetum in a northern Swedish lake: dry weight loss and colonization by macroinvertebrates. J. Ecol., 67: 191--200. Davis, C.B. and Van Der Valk, A.G., 1983. Uptake and release of nutrients by living and decomposing Typha glauca Godr. tissues at Eagle Lake, Iowa. Aquat. Bot., 16: 75--89. DeMarte, J.A. and Hartman, R.T., 1974. Studies of absorption of 32p, SgFe ' and 45Ca by watermilfoil (Myriophyllum exalbescens Fenald). Ecology, 55: 188--194. Drifmeyer, J.E., Thayer, G.W., Cross, F.A. and Zieman, J.C., 1980. Cycling of Mn, Fe, Cu, and Zn by eelgrass, Zoster, marina, L. Am. J. Bot., 67 : 1089--1096. Environmental Protection Agency, 1971. Methods for Chemical Analysis of Water Waste. U S. Government Printing Office, 312 pp. Fassett, N.C., 1972. A Manual of Aquatic Plants. University of Wisconsin Press, Milwaukee, Wisconsin, 405 pp. Godshalk, G.L. and Wetzel, R.G., 1978. Decomposition of aquatic angiosperms. II. Particulate components. Aquat. Bot., 5: 301--327. Good, R.E. and Good, N.F., 1975. Vegetation and production o f the Woodbury CreekHessian Run freshwater tidal marshes. Bartonia, 43: 38--45. Heslop-Harrison, Y., 1955. Biological flora of the British Isles. Nuphar Sin. J. Ecol., 43: 324--364. Hutchinson, G . E , 1975. A Treatise of Limnology. III. Limnological Botany. Wiley, New York, 660 pp. Kimball, K.D. and Baker, A.L., 1982. Variations in the mineral content o f Myriophyllum heterophyllum Michx. related to site and season. Aquat. Bot., 14: 139--149. Kimball, K.D. and Baker, A.L., 1983. Temporal and morphological factors related to mineral composition in Myriophyllum heterophyllum Michx. Aquat. Bot., 16: 189-205. Kistritz, R.U., 1978. Recycling of nutrients in an enclosed aquatic c o m m u n i t y of decomposing macrophytes (Myriophyllum spicatum). Oikos, 30: 561--569. K o r m o n d y , E J., 1968. Weight loss of cellulose and aquatic macrophytes in a Carolina Bay. Limnol. Oceanogr., 13: 522--526. Moeller, R.E., 1978. Seasonal changes in biomass, tissues chemistry, and net production of the evergreen h y d r o p h y t e , Lobelia dortmanna. Can. J. Bot., 56: 1425--1433. Moeller, R.E., 1980. The temperature-determined growing season of a submerged hydrophyte: tissue chemistry and biomass turnover of Utricularia purpurea. Freshwater Biol., 10: 391--400. Nichols, D.S. and Keeney, D.R., 1973. Nitrogen and phosphorus release from decaying water milfoil. Hydrobiologia, 42: 509--525. Nichols, D.S. and Keeney, D.R., 1976. Nitrogen nutrition of Myriophyllum spicatum: variation of plant tissue nitrogen concentration with season and site in Lake Wingra. Freshwater Biol., 6: 137--144. Nichoison, S.A. and Best, D.G., 1974. Root: shoot and leaf area relationships of macrophyte communities in Chantau qua Lake, New York. Bull. Torrey Bot. Club, 101: 96--100. Penfound, W.T., 1956. Primary production of vascular aquatic plants. Limnol. Oceanogr., 1 : 92--101.
252 Rich, P.H., Wetzel, R.G. and Thuy, N.V., 1971. Distribution, production and role of aquatic macrophytes in a southern Michigan marl lake. Freshwater Biol., 1: 3--21. Riemer, D.N. and Toth, S.J., 1970. Chemical composition of five species of Nymphaeaceae. Weed Sci., 18: 4--6. Sand-Jensen, K. and S~ndergaard, M., 1978. Growth and production of isoetids in oligotrophic Lake Kalgaard, Denmark. Verh. Int. Ver. Theor. Angew. Limnol., 20: 659-666. SAS Institute Inc., 1982. SAS User's Guide: Statistics. SAS Institute Inc., Cary, NC. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular Plants. Edward Arnold, London, 610 pp. Twilley, R.R., 1976. Phosphorus cycling in Nuphar luteum communities in the lower Chowan River, North Carolina. M.S. Thesis, East Carolina University, 119 pp. Twilley, R.R., Brinson, M.M. and Davis, G.J., 1977. Phosphorus absorption, translocation and secretion in Nuphar luteum. Limnol. Oceanogr., 22: 1022--1032. Waring, T.G., 1970. Primary production of the emergent h y d r o p h y t e , Nuphar advena. Ph.D. Thesis, University of Pittsburgh. Westlake, D.F., 1965a. Some basic data for investigations of the productivity of aquatic macrophytes. In: C.R. Goldman (Editor), Primary Productivity in Aquatic Environments. Mem. Inst. Ital. Idrobiol., 18 Suppl., University of California Press, Berkeley, California, pp. 229--248. Westlake, D.F., 1965b. Theoretical aspects of comparability of productivity data. In: C.R. Goldman (Editor), Primary Productivity in Aquatic Environments. Mere. Inst. Ital. Idrobiol., 18 Suppl., University of California Press, Berkeley, California. Wetzel, R.G., 1975. Limnology. Saunders, Philadelphia, 743 pp. Whigham, D.F., McCormack, J., G o o d , R.E. and Simpson, R.L., 1978. Biomass and primary production in freshwater tidal wetlands o f the middle Atlantic Coast. In: R.E. Good, D.F. Whigham and R.L. Simpson (Editors), Freshwater Wetlands: Ecological Processes and Management Potential. Academic Press, New York, pp. 3--20. Whigham, D.F. and Simpson, R.L., 1978. The relationship between above-ground and below-ground biomass of freshwater tidal wetland macrophytes. Aquat. Bot., 5: 355-364.
